Domoic Acid Toxicity In California Sea Lions (Zalophus Californianus) Stranded Along The Central California Coast, May - October 1998
Gulland, F. (2000)
Report to the National Marine Fisheries Service Working Group on Unusual Marine Mammal Mortality Events. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-OPR-17, 45p.
Between May 15 and June 19, 1998, 70 California sea lions (Zalophus californianus) and one northern fur seal (Callorhinus ursinus) stranded along the central California coast from San Luis Obispo to San Mateo County. Of these 70 animals, 54 were adult females, with 27 (50 %) pregnant; three were subadult females; two were juvenile females; one was a yearling female; six were subadult males and four were juvenile males (Appendix 1). All animals were in good nutritional condition and displayed similar clinical signs that were predominantly neurological. The animals had severe seizures that either became increasingly frequent, resulting in opisthotonus, then death, or became less frequent with the animals showing ataxia and decreased responsiveness to stimuli between seizures and eventually becoming clinically normal. Forty-eight of the 70 animals (69 %) died despite treatment.
Treatment consisted of supportive care with oral and subcutaneous fluids, antibiotic cover with penicillin, control of seizures using diazepam, lorazepan, and phenobarbitone, and reduction of cerebral edema using dexamethasone. Induction of parturition using dexamethasone and prostaglandin F2a was attempted in adult females with open cervices and dead intrauterine fetuses.
Hematological parameters in these stranded sea lions were within normal limits, as were serum biochemical profiles other than creatine kinase levels. The creatine kinase levels were elevated in most animals, presumably as a consequence of muscular damage during seizures. Levels of blood lead were normal in the eight affected animals tested, and brain cholinesterase levels were normal in the five affected animals tested.
Virus neutralization (VN) tests for phocine distemper virus (PDV) detected low levels of antibody in 10 of 34 animals (29 %). After two weeks, four of these 10 animals showed low positive, but rising, titers on VN. No signs of respiratory disease or novel neurologic signs were detected. After a further month, these four animals were seronegative to PDV. Three animals that had been in contact with seropositive animals remained seronegative. A retrospective survey of banked sera from 100 adult California sea lions that had stranded previously revealed that 20 % had low titers to PDV.
A variety of non-specific lesions were observed on gross post mortem examination. These included gastric ulceration and erosion with associated lymphadenopathy, bile stasis, pulmonary congestion and occasional subcutaneous hemorrhages. Sea lions that died within the first two days of stranding had diffusely pale myocardium with occasional focal areas of severe pallor. All pregnant females had necrotic placentae and dead fetuses.
Bacteria isolated from tissues at post mortem were typical of those isolated from stranded California sea lions in recent years. A novel calicivirus was isolated from myocardium of one animal (#3709).
The predominant histologic lesion in affected animals was neuronal necrosis, that was most severe in zones CA3 and CA4 of hippocampi and the dentate gyri. There were also intramyelinic and neuropil edema and occasional foci of gliosis. In some animals that died within 48 hours of stranding, there was multifocal myocardial necrosis and inflammation.
Domoic acid, a biotoxin produced by a diatom, was detected in serum of 3 of 7 animals, urine of 7 of 14 animals, and feces of 3 of 9 animals. Two of the positive fecal samples were examined by electron microscopy, and frustules of Pseudo-nitzschia australis were observed. No domoic acid was found in kidney, stomach washings, cerebrospinal fluid, or brain samples from affected animals. Analyses were carried out using a receptor binding assay (RBA) and High Performance Liquid Chromatography with Ultraviolet detection (HPLC/UV). HPLC/mass spectrometry (HPLC/MS and HPLC/MS/MS) carried out on a subset of samples from each tissue type provided independent confirmation of the chemical identity of the biotoxin.
A bloom of Pseudo-nitzschia australis (P. australis) occurred in Monterey Bay during the latter half of May 1998, reaching its peak on or about May 22. The greatest concentration of P. australis recorded was ~200,000 cells per liter. Cells were concentrated near shore, possibly in response to nutrients of terrestrial origin brought to coastal waters by enhanced river outflow. Plankton samples were also analyzed for domoic acid using a receptor binding assay. The rise and fall of domoic acid in these samples corresponded to the rise and fall of P. australis observed in the plankton. Anchovies collected from the bay on May 22, 1998 had levels of domoic acid of 105.6 mg domoic acid/g tissue, whereas fish collected on June 10, 1998 had no detectable levels of domoic acid. Anchovies collected during the peak of the P. australis bloom that contained high amounts of domoic acid had P. australis frustules within their stomachs. In Monterey Bay, the bloom of P. australis was followed by a bloom of P. pseudodelicatissima. Anchovies collected from Monterey Bay reflected this change in species abundance in their stomach contents. No P. australis frustules or domoic acid were detected in stomach contents of these fish, and no domoic acid was detected in the plankton during the P. pseudodelicatissima bloom.
Three of the 23 sea lions (#3815, #3822 and #3815) that survived treatment during the event in May and June 1998 were equipped with satellite and radio-transmitters prior t their release on November 15, 1998. Battery life of the satellite transmitters was three months. Satellite and re-sight data indicated that sea lions survived for at least 48, 64 and 94 days respectively. Two sea lions traveled as far south as the Channel Islands, whereas the third sea lion remained in the vicinity of Ano Nuevo Island. All three sea lions that were sighted during the three-month telemetry period appeared healthy and displayed normal behavior.
During routine surveys around the Monterey Bay during the months of May and June 1998, a 3.5 fold increase in numbers of dead beach-cast birds and pinnipeds was detected to compare to the same months of the previous year. The majority of the dead birds were Common Murres, Surf Scoters and Sooty Shearwaters. Large numbers of stranded sea lions were also detected along other central California beaches at the time. The extent to which these mortalities was due to domoic acid toxicity rather than as a consequence of starvation due to El Nino conditions is unclear, since most animals were not examined.
From July 2 to October 17, 1998, an additional 11 California sea lions stranded displaying similar clinical sign to those that stranded during late May and early June. Nine of these animals stranded between October 3 and October 17. Four animals survived and seven died. The dead animals had histologic lesions similar to those in the earlier cases. Domoic acid was detected in urine of two of these animals by the microplate assay. At the same time (early October), cells of P. australis were observed in Monterey Bay around the Santa Cruz and Capitola piers, but were at relatively low concentrations (<10,000 cells per liter). However, further offshore (outside Monterey Bay), concentrations of P. australis were in excess of 100,000 cells per liter. It is likely that the source of domoic acid affecting sea lions during October was a bloom outside of Monterey Bay.
In summary, the combination of clinical signs, histopathological, toxicological, epidemiological and oceanographic changes led to the conclusion that domoic acid toxicity was the cause of this Marine Mammal Unusual Mortality Event. Domoic acid was first reported as a cause of toxicity in humans in 1987, when four people died and approximately one hundred were clinically ill following ingestion of contaminated mussels on the Prince Edward Island, Canada. This event is the first documented occurrence of domoic acid toxicity in marine mammals.