Elizabeth R. Frame

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.

A novel antibody-based biomarker for chronic algal toxin exposure and sub-acute neurotoxicity

The neurotoxic amino acid, domoic acid (DA), is naturally produced by marine phytoplankton and presents a significant threat to the health of marine mammals, seabirds and humans via transfer of the toxin through the foodweb. In humans, acute exposure causes a neurotoxic illness known as amnesic shellfish poisoning characterized by seizures, memory loss, coma and death. Regular monitoring for high DA levels in edible shellfish tissues has been effective in protecting human consumers from acute DA exposure. However, chronic low-level DA exposure remains a concern, particularly in coastal and tribal communities that subsistence harvest shellfish known to contain low levels of the toxin. Domoic acid exposure via consumption of planktivorous fish also has a profound health impact on California sea lions (Zalophus californianus) affecting hundreds of animals yearly. Due to increasing algal toxin exposure threats globally, there is a critical need for reliable diagnostic tests for assessing chronic DA exposure in humans and wildlife. Here we report the discovery of a novel DA-specific antibody response that is a signature of chronic low-level exposure identified initially in a zebrafish exposure model and confirmed in naturally exposed wild sea lions. Additionally, we found that chronic exposure in zebrafish caused increased neurologic sensitivity to DA, revealing that repetitive exposure to DA well below the threshold for acute behavioral toxicity has underlying neurotoxic consequences. The discovery that chronic exposure to low levels of a small, water-soluble single amino acid triggers a detectable antibody response is surprising and has profound implications for the development of diagnostic tests for exposure to other pervasive environmental toxins.

Chronic low-level domoic acid exposure alters gene transcription and impairs mitochondrial function in the CNS

Domoic acid is an algal-derived seafood toxin that functions as a glutamate agonist and exerts excitotoxicity via overstimulation of glutamate receptors (AMPA, NMDA) in the central nervous system (CNS). At high (symptomatic) doses, domoic acid is well-known to cause seizures, brain lesions and memory loss; however, a significant knowledge gap exists regarding the health impacts of repeated low-level (asymptomatic) exposure. Here, we investigated the impacts of low-level repetitive domoic acid exposure on gene transcription and mitochondrial function in the vertebrate CNS using a zebrafish model in order to: (1) identify transcriptional biomarkers of exposure; and (2) examine potential pathophysiology that may occur in the absence of overt excitotoxic symptoms. We found that transcription of genes related to neurological function and development were significantly altered, and that asymptomatic exposure impaired mitochondrial function. Interestingly, the transcriptome response was highly variable across the exposure duration (36 weeks), with little to no overlap of specific genes across the six exposure time points (2, 6, 12, 18, 24, and 36 weeks). Moreover, there were no apparent similarities at any time point with the gene transcriptome profile exhibited by the glud1 mouse model of chronic moderate excess glutamate release. These results suggest that although the fundamental mechanisms of toxicity may be similar, gene transcriptome responses to domoic acid exposure do not extrapolate well between different exposure durations. However, the observed impairment of mitochondrial function based on respiration rates and mitochondrial protein content suggests that repetitive low-level exposure does have fundamental cellular level impacts that could contribute to chronic health consequences.

Does the Columbia River plume influence phytoplankton community structure along the Washington and Oregon coasts

[1] As part of the River Influences on Shelf Ecosystems (RISE) program, we examined the influence of the Columbia River plume on the composition and biomass of phytoplankton communities on the Washington and Oregon coasts. We determined the taxonomic composition, size structure, and biomass of phytoplankton assemblages in near-surface shelf waters during four 3-week cruises in spring and/or summer of 2004–2006. As the Columbia plume is very dynamic, the influence of the plume was examined in three ways. Two comparisons of the entire data set were made: (1) a geographical comparison of the Washington, Oregon, and Columbia River mouth regions based on latitude and (2) a ‘‘plume’’ versus ‘‘nonplume’’ comparison based on salinity. A third comparison focused on samples taken in and outside of three specific plumes under different upwelling/downwelling conditions. In whole data set comparisons, there were no significant differences in chlorophyll, carbon biomass, or diatom community structure between regions or between plume and nonplume samples. However, within some cruises there were regional and plume differences in chlorophyll and biomass. Diatom community composition differed between cruises, but within a cruise it was similar across regions and in plume/nonplume samples, indicating there was no unique plume community. On finer time and space scales, differences in community structure as well as biomass were evident between samples in and outside of specific plumes. Over broader scales, the Columbia plume acts to make coastal phytoplankton communities more homogeneous. Specific impacts will depend on the history of upwelling and nutrient status of the coastal waters which the plume encounters.

Correction to Planktonic growth and grazing in the Columbia River plume region: A biophysical model study

A four-box model of planktonic nutrient cycling was coupled to a high-resolution hindcast circulation model of the Oregon-Washington coast to assess the role of the Columbia River plume in shaping regional-scale patterns of phytoplankton biomass and productivity. The ecosystem model tracks nitrogen in four phases: dissolved nutrients, phytoplankton biomass, zooplankton biomass, and detritus. Model parameters were chosen using biological observations and shipboard process studies from two cruises in 2004 and 2005 conducted as part of the RISE (River Influences on Shelf Ecosystems) program. In particular, community growth and grazing rates from 26 microzooplankton dilution experiments were used, in conjunction with analytical equilibrium solutions to the model equations, to diagnose key model rate parameters. The result is a simple model that reproduces both stocks (of nutrients, phytoplankton, and zooplankton) and rates (of phytoplankton growth and microzooplankton grazing) simultaneously. Transient plume circulation processes are found to modulate the Washington-Oregon upwelling ecosystem in two ways. First, the presence of the plume shifts primary production to deeper water: under weak or variable upwelling winds, 20% less primary production is seen on the inner shelf and 10-20% more is seen past the 100 m isobath. River effects are smaller when upwelling is strong and sustained. Second, increased retention in the along-coast direction (i.e., episodic interruption of equatorward transport) causes a net shift toward older communities and increased micrograzer impact on both the Oregon and Washington shelves, from the mid-shelf seaward.