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The Science of the NOAA Marine Biotoxins Program’s “ART”

The National Centers for Coastal and Ocean Science (NCCOS) “ART” program has been working out of the Charleston, S.C., based NOAA Marine Biotoxins Program for more than a decade. The ART team, under the supervision of John Ramsdell, uses highly sophisticated instruments and techniques to provide timely analytical support on unusual mortality events and human illnesses associated with harmful algal blooms. NCCOS management recently conducted a remote “roundtable discussion” with a number of key ART personnel to provide practical insights into the operations of this unique resource:

Analytic Response Team (ART) Technicians performing bioassays at CCEHBRLorraine, the letters “ART” mean different things to different people. Can you explain just what ART – the Analytical Response Team – is?

Lorraine Creel, ART Specialist: Confirming algal toxins has always been difficult because there are so many uncertainties, everything ranging from non-specific symptoms and the inherent complexity of toxin detection to the unknown impacts on affected species.

To meet this challenge, NOAA’s Marine Biotoxins Program established a harmful algal bloom Analytical Response Team, or “ART.” Our team provides scientific guidance and identification of harmful algae and their toxins during suspected harmful algal blooms, during marine animal mortality events, and also during human poisonings.

Who exactly do you mean by “our team” here, Lorraine? Can you give us a sense of the people who make up ART?

Creel: The ART is composed of a multi-disciplinary team of scientists along with an event coordinator. Together, they are responsible for designing and implementing an event-specific solution to identify toxins associated with harmful algal blooms.

The team combines expertise in algal taxonomy, toxicology, and toxin chemistry, and it’s that combination of skills that makes it possible for us to solve most events associated with harmful algal blooms. Our commitment is to supply accurate information in a timely manner. That way, we allow managers to make informed decisions involving shellfish harvests, life support for marine mammals, beach closures, and other remedial actions.

Tod, Lorraine has introduced this event coordinator responsibility to us: Can you elaborate on that position and on ART’s specific capabilities?

Tod Leighfield, ART Coordinator: The ART scientists’ broad expertise can be drawn upon to investigate most events associated with harmful algal blooms and the toxins they produce. The strength of this group comes from its use of sophisticated analyses to detect the presence of algal toxins across many toxin classes.

Specifically we use a two-step approach to analysis. We first screen samples using fast, toxin-specific detection methods, and then confirm the presence of individual toxins using analytical instruments.

Let’s say we’re out in the field and we suspect a HAB event and need your assistance.

Leighfield: The ART is contacted through any one of the Marine Biotoxins Program scientific staff. We call these scientists “early event listeners”. Early event listeners extensively network with other coastal stewards who study harmful algae as well as other coastal species.

But how does ART then decide whether or not to respond to a request?

Leighfield: Our team uses a sense-interpret-decide decision process. Because each event is unique, we have to determine an event-specific solution. Once contacted, the ART team meets as a group and determines its capabilities to address the questions. If the team has the appropriate resources to help address the problem, we begin the analyses. After it completes and reviews the analyses, the ART team provides its results to the person requesting its assistance, and also to other affiliated groups.

Let’s look at the actual testing that ART might do in a particular case. Peter, as a chemist with the ART group, can you discuss both the instrument-based tests ART uses and also the animal-based tests? Is one necessarily better than the other?

Peter Moeller. Research Chemist: No, we regularly use both approaches in a complementary fashion. Animal-based tests, commonly called bioassays, use continuously propagated animal cells in culture dishes and provide a broad measure of the presence of toxins. Instrumental analysis by mass spectrometry is typically used afterwards and provides identification and measurement of specific toxin molecules present in a sample.

So are the results comparable across different toxins?

Moeller: Not necessarily, because a given class of toxins often can be manifested as many different individual chemical structures.

Bioassays detect the combined toxic activity of a number of co-occurring chemical structures for a given toxin class. On the other hand, analytical measurements are highly specific and provide defined “fingerprints” for the precise chemical structures we are looking for.

Marine Biotoxins Program staff mass based analysis of marine toxinsHow does ART decide which type of test to use? Why one rather than the other?

Moeller: We typically use bioassays to first identify whether a given class of toxin is present. The bioassay provides a single value that relates well to toxicity. That way, we can have an idea about the hazard posed by the toxin.

We next use the analytical measurement to identify which specific chemical structures are present. Absolute chemical identity is needed for a number of purposes, particularly for those decisions involving protected species or those that have economic impact.

Can we consider the kinds of animal mortality events that have occurred in recent years in California? Are there historical records to suggest that such marine animal mortality events have also occurred in the past?

Gregory Doucette, Research Oceanographer: The domoic acid-related, sea lion mortality event in 1998 was the first to be confirmed using analytical methods. But there have been many other documented cases dating back to at least 1978, and in those events, sea lions and other mammals such as northern fur seals displayed behavioral and clinical symptoms consistent with domoic acid poisoning.

Because many marine birds consume some of the same plankton-eating fish that sea lions do, it’s not surprising that in 1992 a mortality event involving pelicans and cormorants was also linked to domoic acid exposure.

Let me point to an interesting anecdote, one that suggests that the bizarre behavior of the birds in Alfred Hitchcock’s famous 1963 film, “The Birds,” was based on the neurological symptoms observed during a possible domoic acid poisoning event. In that case, a Santa Cruz newspaper reported that large numbers of birds had inexplicably crashed into houses along the California coast.

Transport of domoic acid intoxicated California Sea Lion for rehabilitation by the Marine Mammal Center in Sausalito, CATalk a moment about the geography of these events. Are there geographical trends to these mortality events?

Doucette: In the past, most of the reported marine mammal mortality events associated with algal toxins have occurred along the central California coast, frequently focused in and adjacent to the Monterey Bay area.

However, in recent years, stranding and mortalities of marine mammals, including both cetaceans and pinnipeds, have been more widespread. A 2002 episode, the second largest marine mammal mortality event ever recorded in the U.S., reached well into southern California waters.

Since domoic acid producing algae occur all along the west coast of Central and North America, the potential for mortality events tends to be influenced more by the movement and feeding behavior of the animals.

And are there climate-based trends to these mortality events?

Doucette: It does appear that there can be an influence of climatic factors such as El Niño Southern Oscillation (ENSO) events. But this is more of an indirect rather than a direct effect on the marine mammals.

For example, during strong El Niño periods, warmer and generally less productive water from the south tends to move north along the California coast. This can affect the phytoplankton community by favoring the growth of algae not known to produce domoic acid, although blooms of domoic acid producing species can occur rapidly if conditions change.

It is important to realize that marine mammals can also suffer from a lack of food during these periods of low productivity. So we must take this into account when evaluating a mortality event and rely on analytical methods to demonstrate that animals were exposed to domoic acid.

Well, are these mortality events in the United States limited to the West Coast? Do you find them also on the East Coast?

Frances Van Dolah, Analytical Response Management Team Leader: Yes, in the summer of 1987 and into early 1988, hundreds of bottlenose dolphins died along the eastern seaboard. The initial report indicated that eating fish contaminated with brevetoxin had poisoned the animals.

However, that report was never substantiated. That mortality event proved to be a defining moment, emphasizing a need for a national program that could provide accurate information on algal toxins during unusual mortality events.

Do the eastern seaboard events involve the same toxins as those on the west coast?

Van Dolah: The east coast events involve largely different toxins.

In the northeast, for instance, saxitoxins were implicated in a humpback whale mortality in 1988. In Florida, brevetoxins have been implicated in deaths of bottlenose dolphins and manatees.

And what about the factors leading to these events? Do those too differ from east to west coast?

Van Dolah: In each case, the causative algal species is a naturally occurring organism in the environment where the mortalities occurred. And remember that although blooms occur on an annual cycle, they don’t always result in mortality events.

Interestingly, in most cases a mortality event can be correlated with the co-incidence of secondary factors. For example, in a recent case of domoic acid poisonings on the west coast, a climatic shift corresponded with a change in distribution of certain prey organisms and the toxic algae. In the case of the manatee mortalities in Florida, unusually low rainfall in 1996 resulted in high salinity. That increased salinity allowed the blooms to persist in estuarine waters through which the manatees migrate at a certain time of the year, and they were exposed to high levels of toxin. In the case of the humpback whales, an unusual juxtaposition of prey species and toxic blooms may have been key to their exposure.

On a larger scale, recent evidence suggests that climate and productivity of the Pacific Ocean change with a cycle of approximately 50 years. The recent domoic acid poisonings on the west coast correspond temporarily with a climate shift that favors high productivity cooler water species, including anchovies, which were the foodweb vector that transferred the toxin from the algae to the sea lions. If this correlation proves true, we might expect more mortality events of this nature on the west coast.

Is all of the ART work done remotely from the Charleston facility? Or does it also involve field work?

Stephan Morton, Oceanographer: In some cases, personnel from the Charleston-based Marine Biotoxins Program travel to the case site.

For example, the State of Maine requested assistance to investigate reports of the possibility of Diarrhetic Shellfish Poisoning (DSP). ART scientists traveled to Maine and through a number of field observations and analytical techniques, located both the source organism and the toxin responsible for DSP. The Maine Department of Natural Resources now samples these sites for the organisms and their toxins as part of its routine monitoring of shellfish toxins.

And is all of the ART’s work domestic, or are its services also in demand abroad?

Morton: The ART does respond to events outside the US when requested. For example, a couple of years ago a number of people in Russia displayed symptoms of DSP from eating mussels collected from the Black Sea.

In that case, Dr. Alexander Vershinin, of the Shirshov Institute of Oceanology, contacted the Marine Biotoxins Program. With financial support from the U.S. Civilian Research Development Foundation, his group worked with the ART to investigate the problem. NOAA scientists traveled to the Russian Black Sea coast for two months to sample areas prone to DSP outbreaks, and Dr. Vershinin traveled to the U.S. to help conduct analyses at the NOAA laboratory.

The research conducted during this time not only detected the organisms that cause DSP, but also detected other potentially toxic species that have human health consequences.

Collecting plankton samples for potentially harmful microalgaeHow does the ART work differ when it is conducted outside the Charleston facility?

Morton: The work conducted outside the facility really is two-fold.

First, we travel to the site to examine the local plankton community for the presence of potentially toxic species and examine the shellfish population for the presence of algal toxins.

In addition to conducting these field and laboratory experiments, we then help design monitoring strategies and teach local personnel various methods such as plankton collection, identification, and toxin analysis.

Are there examples of particularly unusual investigative wildlife work that the ART recently has done?

Leighfield: Well, one involves our national bird, the bald eagle.

We currently are investigating the hypothesis that an algal toxin may be responsible for bald eagle mortalities. The eagle mortalities are related to a neurological disease called avian vacuolar myelinopathy. It has been observed in duck and birds of prey on southeastern US inland reservoirs. The ART is working with state resource managers to identify potential toxins in algae that the ducks are feeding on.

And can you comment also on investigative work the ART team is doing on unusual or unexplained human mortalities?

Leighfield: Yes, in fact in April 2002 there was a case of poisoning in the coastal town of Bolinao located on a pristine bay in the northern Philippines. Fish farming had just recently been introduced there.

Three people had died, the oldest just 18 years old, and several others became ill after eating a seaweed locally prepared as a salad known as “kulot”. The ART was contacted to determine if the seaweed might have contained a marine toxin. A scientist from the Philippines traveled to the Marine Biotoxins laboratory and worked with ART scientists conducting different tests for toxins.

And were you able to find an answer? Do you always succeed in finding your answer?

Leighfield: In the case of the Philippine deaths, we in fact were unable to identify a specific algal toxin. However, we were able to rule out many of the common algal toxins, and even a few of the less common toxins. This information allowed the local public health officials to direct their resources to look further into rarer causes of the mortalities.

Can you explain why precisely local partners need ART’s expertise? Why can’t they make these determinations on their own or through local or regional experts?

Van Dolah: In the case of marine mammals, the people dealing on-site with mortality events usually are experts in marine mammal health, and they are generally not equipped to conduct analysis of algal toxins. The ART provides that specialized expertise on a no-cost basis as a service to the NMFS Office of Protected Species, Marine Mammal Unusual Mortality Event Working Group. This group was assembled because of the complexities involved in determining causes of morbidity and mortality, with algal toxins being only one issue at hand.

As Peter mentioned earlier, unambiguously identifying algal toxins is difficult because of their unusual structures and complex mixtures. That’s particularly the case when testing biological samples such as marine mammal tissues.

Rapid test kits, targeted primarily for water and shellfish analysis, are becoming commercially available. But these tests are not designed for marine mammal samples and cannot provide definitive toxin identification. The Marine Biotoxin Program’s ART has both expertise in the analysis of all algal toxin classes and the experience to design analyses as well as interpret findings in perspective to past case studies. That’s what makes it such a unique and valuable national resource in figuring out these harmful events.

“ART at Work” provides information on some specific cases.

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