Teri Rowles

Mortality of sea lions along the central California coast linked to a toxic diatom bloom.

Over 400 California sea lions (Zalophus californianus) died and many others displayed signs of neurological dysfunction along the central California coast during May and June 1998. A bloom of Pseudo-nitzschia australis (diatom) was observed in the Monterey Bay region during the same period. This bloom was associated with production of domoic acid (DA), a neurotoxin that was also detected in planktivorous fish, including the northern anchovy (Engraulis mordax), and in sea lion body fluids. These and other concurrent observations demonstrate the trophic transfer of DA resulting in marine mammal mortality. In contrast to fish, blue mussels (Mytilus edulus) collected during the DA outbreak contained no DA or only trace amounts. Such findings reveal that monitoring of mussel toxicity alone does not necessarily provide adequate warning of DA entering the food web at levels sufficient to harm marine wildlife and perhaps humans.

Bottlenose Dolphins as Marine Ecosystem Sentinels: Developing a Health Monitoring System

Bottlenose dolphins (Tursiops truncatus), as long-lived, long-term residents of bays, sounds, and estuaries, can serve as important sentinels of the health of coastal marine ecosystems. As top-level predators on a wide variety of fishes and squids, they concentrate contaminants through bioaccumulation and integrate broadly across the ecosystem in terms of exposure to environmental impacts. A series of recent large-scale bottlenose dolphin mortality events prompted an effort to develop a proactive approach to evaluating risks by monitoring living dolphin populations rather than waiting for large numbers of carcasses to wash up on the beach. A team of marine mammal veterinarians and biologists worked together to develop an objective, quantitative, replicable means of scoring the health of dolphins, based on comparison of 19 clinically diagnostic blood parameters to normal baseline values. Though the scoring system appears to roughly reflect dolphin health, its general applicability is hampered by interlaboratory variability, a lack of independence between some of the variables, and the possible effects of weighting variables. High score variance seems to indicate that the approach may lack the sensitivity to identify trends over time at the population level. Potential solutions to this problem include adding or replacing health parameters, incorporating only the most sensitive measures, and supplementing these with additional measures of health, body condition, contaminant loads, or biomarkers of contaminants or their effects that can also be replicated from site to site. Other quantitative approaches are also being explored.

Emergence of Fatal Avian Influenza in New England Harbor Seals

ABSTRACT From September to December 2011, 162 New England harbor seals died in an outbreak of pneumonia. Sequence analysis of postmortem samples revealed the presence of an avian H3N8 influenza A virus, similar to a virus circulating in North American waterfowl since at least 2002 but with mutations that indicate recent adaption to mammalian hosts. These include a D701N mutation in the viral PB2 protein, previously reported in highly pathogenic H5N1 avian influenza viruses infecting people. Lectin staining and agglutination assays indicated the presence of the avian-preferred SAα-2,3 and mammalian SAα-2,6 receptors in seal respiratory tract, and the ability of the virus to agglutinate erythrocytes bearing either the SAα-2,3 or the SAα-2,6 receptor. The emergence of this A/harbor seal/Massachusetts/1/2011 virus may herald the appearance of an H3N8 influenza clade with potential for persistence and cross-species transmission. IMPORTANCE The emergence of new strains of influenza virus is always of great public concern, especially when the infection of a new mammalian host has the potential to result in a widespread outbreak of disease. Here we report the emergence of an avian influenza virus (H3N8) in New England harbor seals which caused an outbreak of pneumonia and contributed to a U.S. federally recognized unusual mortality event (UME). This outbreak is particularly significant, not only because of the disease it caused in seals but also because the virus has naturally acquired mutations that are known to increase transmissibility and virulence in mammals. Monitoring the spillover and adaptation of avian viruses in mammalian species is critically important if we are to understand the factors that lead to both epizootic and zoonotic emergence. The emergence of new strains of influenza virus is always of great public concern, especially when the infection of a new mammalian host has the potential to result in a widespread outbreak of disease. Here we report the emergence of an avian influenza virus (H3N8) in New England harbor seals which caused an outbreak of pneumonia and contributed to a U.S. federally recognized unusual mortality event (UME). This outbreak is particularly significant, not only because of the disease it caused in seals but also because the virus has naturally acquired mutations that are known to increase transmissibility and virulence in mammals. Monitoring the spillover and adaptation of avian viruses in mammalian species is critically important if we are to understand the factors that lead to both epizootic and zoonotic emergence.

Deadly diving? Physiological and behavioural management of decompression stress in diving mammals

Decompression sickness (DCS; ‘the bends’) is a disease associated with gas uptake at pressure. The basic pathology and cause are relatively well known to human divers. Breath-hold diving marine mammals were thought to be relatively immune to DCS owing to multiple anatomical, physiological and behavioural adaptations that reduce nitrogen gas (N2) loading during dives. However, recent observations have shown that gas bubbles may form and tissue injury may occur in marine mammals under certain circumstances. Gas kinetic models based on measured time-depth profiles further suggest the potential occurrence of high blood and tissue N2 tensions. We review evidence for gas-bubble incidence in marine mammal tissues and discuss the theory behind gas loading and bubble formation. We suggest that diving mammals vary their physiological responses according to multiple stressors, and that the perspective on marine mammal diving physiology should change from simply minimizing N2 loading to management of the N2 load. This suggests several avenues for further study, ranging from the effects of gas bubbles at molecular, cellular and organ function levels, to comparative studies relating the presence/absence of gas bubbles to diving behaviour. Technological advances in imaging and remote instrumentation are likely to advance this field in coming years.

Individual-Based Model Framework to Assess Population Consequences of Polychlorinated Biphenyl Exposure in Bottlenose Dolphins

Marine mammals are susceptible to the effects of anthropogenic contaminants. Here we examine the effect of different polychlorinated biphenyl (PCB) accumulation scenarios on potential population growth rates using, as an example, data obtained for the population of bottlenose dolphins from Sarasota Bay, Florida. To achieve this goal, we developed an individual-based model framework that simulates the accumulation of PCBs in the population and modifies first-year calf survival based on maternal blubber PCB levels. In our example the current estimated annual PCB accumulation rate for the Sarasota Bay dolphin population might be depressing the potential population growth rate. However, our predictions are limited both by model naivety and parameter uncertainty. We emphasize the need for more data collection on the relationship between maternal blubber PCB levels and calf survivorship, the annual accumulation of PCBs in the blubber of females, and the transfer of PCBs to the calf through the placenta and during lactation. Such data require continued efforts directed toward long-term studies of known individuals in wild and semi-wild populations.

Life history as a source of variation for persistent organic pollutant (POP) patterns in a community of common bottlenose dolphins (Tursiops truncatus) resident to Sarasota Bay, FL

As apex predators within coastal ecosystems, bottlenose dolphins (Tursiops truncatus) are prone to accumulate complex mixtures of persistent organic pollutants (POPs). While substantial variations in POP patterns have been previously observed in dolphin populations separated across regional- and fine-scale geographic ranges, less is known regarding the factors influencing contaminant patterns within localized populations. To assess the variation of POP mixtures that occurs among individuals of a population, polychlorinated biphenyl (PCB), organochlorine pesticide (OCP) and polybrominated diphenyl ether (PBDE) concentrations were measured in blubber and milk of bottlenose dolphins resident to Sarasota Bay, FL, and principal components analysis (PCA) was used to explain mixture variations in relation to age, sex and reproductive maturity. PCA demonstrated significant variations in contaminant mixtures within the resident dolphin community. POP patterns in juvenile dolphins resembled patterns in milk, the primary diet source, and were dominated by lower-halogenated PCBs and PBDEs. A significant correlation between principal component 2 (PC2) and age in male dolphins indicated that juvenile contaminant patterns gradually shifted away from the milk-like pattern over time. Metabolically-refractory PCBs significantly increased with age in male dolphins, whereas PCBs subject to cytochrome p450 1A1 metabolism did not, suggesting that changes in male POP patterns likely resulted from the selective accumulation of persistent POP congeners. Changes to POP patterns were gradual for juvenile females, but changed dramatically at reproductive maturity and gradually shifted back towards pre-parturient profiles thereafter. Congener-specific blubber/milk partition coefficients indicated that lower-halogenated POPs were selectively offloaded into milk and changes in adult female contaminant profiles likely resulted from the offloading of these compounds during the first reproductive event and their gradual re-accumulation thereafter. Overall, these results indicate that significant variations in contaminant mixtures can exist within localized populations of bottlenose dolphins, with life history factors such as age and sex driving individual differences.

Bottlenose dolphins as indicators of persistent organic pollutants in the western North Atlantic Ocean and northern Gulf of Mexico.

Persistent organic pollutants (POPs) including legacy POPs (PCBs, chlordanes, mirex, DDTs, HCB, and dieldrin) and polybrominated diphenyl ether (PBDE) flame retardants were determined in 300 blubber biopsy samples from coastal and near shore/estuarine male bottlenose dolphins (Tursiops truncatus) sampled along the U.S. East and Gulf of Mexico coasts and Bermuda. Samples were from 14 locations including urban and rural estuaries and near a Superfund site (Brunswick, Georgia) contaminated with the PCB formulation Aroclor 1268. All classes of legacy POPs in estuarine stocks varied significantly (p < 0.05) among sampling locations. POP profiles in blubber varied by location with the most characteristic profile observed in bottlenose dolphins sampled near the Brunswick and Sapelo estuaries along the Georgia coast which differed significantly (p < 0.001) from other sites. Here and in Sapelo, PCB congeners from Aroclor 1268 dominated indicating widespread food web contamination by this PCB mixture. PCB 153, which is associated with non-Aroclor 1268 PCB formulations, correlated significantly to human population indicating contamination from a general urban PCB source. Factors influencing regional differences of other POPs were less clear and warrant further study. This work puts into geographical context POP contamination in dolphins to help prioritize efforts examining health effects from POP exposure in bottlenose dolphins.

Adrenal Gland and Lung Lesions in Gulf of Mexico Common Bottlenose Dolphins (Tursiops truncatus) Found Dead following the Deepwater Horizon Oil Spill

A northern Gulf of Mexico (GoM) cetacean unusual mortality event (UME) involving primarily bottlenose dolphins (Tursiops truncatus) in Louisiana, Mississippi, and Alabama began in February 2010 and continued into 2014. Overlapping in time and space with this UME was the Deepwater Horizon (DWH) oil spill, which was proposed as a contributing cause of adrenal disease, lung disease, and poor health in live dolphins examined during 2011 in Barataria Bay, Louisiana. To assess potential contributing factors and causes of deaths for stranded UME dolphins from June 2010 through December 2012, lung and adrenal gland tissues were histologically evaluated from 46 fresh dead non-perinatal carcasses that stranded in Louisiana (including 22 from Barataria Bay), Mississippi, and Alabama. UME dolphins were tested for evidence of biotoxicosis, morbillivirus infection, and brucellosis. Results were compared to up to 106 fresh dead stranded dolphins from outside the UME area or prior to the DWH spill. UME dolphins were more likely to have primary bacterial pneumonia (22% compared to 2% in non-UME dolphins, P = .003) and thin adrenal cortices (33% compared to 7% in non-UME dolphins, P = .003). In 70% of UME dolphins with primary bacterial pneumonia, the condition either caused or contributed significantly to death. Brucellosis and morbillivirus infections were detected in 7% and 11% of UME dolphins, respectively, and biotoxin levels were low or below the detection limit, indicating that these were not primary causes of the current UME. The rare, life-threatening, and chronic adrenal gland and lung diseases identified in stranded UME dolphins are consistent with exposure to petroleum compounds as seen in other mammals. Exposure of dolphins to elevated petroleum compounds present in coastal GoM waters during and after the DWH oil spill is proposed as a cause of adrenal and lung disease and as a contributor to increased dolphin deaths.

Relationship between persistent organic pollutants (POPs) and ranging patterns in common bottlenose dolphins (Tursiops truncatus) from coastal Georgia, USA

Bottlenose dolphins (Tursiops truncatus) are apex predators in coastal southeastern U.S. waters; as such they are indicators of persistent organic pollutants (POPs) in coastal ecosystems. POP concentrations measured in a dolphins blubber are influenced by a number of factors, including the animals sex and ranging pattern in relation to POP point sources. This study examined POP concentrations measured in bottlenose dolphin blubber samples (n=102) from the Georgia, USA coast in relation to individual ranging patterns and specifically, distance of sightings from a polychlorinated biphenyl (PCB) point source near Brunswick, Georgia. Dolphin ranging patterns were determined based upon 5years of photo-identification data from two field sites approximately 40km apart: (1) the Brunswick field site, which included the Turtle/Brunswick River Estuary (TBRE), and (2) the Sapelo field site, which included the Sapelo Island National Estuarine Research Reserve (SINERR). Dolphins were categorized into one of three ranging patterns from photo-identification data. Individuals with sighting histories exclusively within one of the defined field sites were considered to have either Brunswick or Sapelo ranging patterns. Individuals sighted in both field sites were classified as having a Mixed ranging pattern. Brunswick males had the highest concentrations of PCBs reported for any marine mammal. The pattern of PCB congeners was consistent with Aroclor 1268, a highly chlorinated PCB mixture associated with a Superfund site in Brunswick. PCB levels in Sapelo males were lower than in Brunswick males, but comparable to the highest levels measured in other dolphin populations along the southeastern U.S. Female dolphins had higher Aroclor 1268 proportions than males, suggesting that the highly chlorinated congeners associated with Aroclor 1268 may not be offloaded through parturition and lactation, as easily as less halogenated POPs. Individuals sighted farther from the Superfund point source had lower Aroclor 1268 proportions.

ASSOCIATION OF AN UNUSUAL MARINE MAMMAL MORTALITY EVENT WITH PSEUDO-NITZSCHIA SPP. BLOOMS ALONG THE SOUTHERN CALIFORNIA COASTLINE

During 2002, 2,239 marine mammals stranded in southern California. This unusual marine mammal stranding event was clustered from April to June and consisted primarily of California sea lions (Zalophus californianus) and long-beaked common dolphins (Delphinus capensis) with severe neurologic signs. Intoxication with domoic acid (DA), a marine neurotoxin produced during seasonal blooms of Pseudo-nitzschia spp., was suspected. Definitively linking harmful algal blooms to large-scale marine mammal mortalities presents a substantial challenge, as does determining the geographic extent, species composition, and potential population impacts of marine mammal die-offs. For this reason, time series cross-correlation analysis was performed to test the temporal correlations of Pseudo-nitzschia blooms with strandings occurring along the southern California coastline. Temporal correlations were identified between strandings and blooms for California sea lions, long-beaked common dolphins, and short-beaked common dolphins (Delphinus delphis). Similar correlations were identified for bottlenose dolphins (Tursiops truncatus) and gray whales (Eschrichtius robustus), but small sample sizes for these species made associations more speculative. The timing of the blooms and strandings of marine mammals suggested that both inshore and offshore foraging species were affected and that marine biotoxin programs should include offshore monitoring sites. In addition, California sea lion-strandings appear to be a very sensitive indicator of DA in the marine environment, and their monitoring should be included in public health surveillance plans.