Domoic Acid Toxicity in California Sea Lions (Zalophus californianus) Stranded Along the Central California Coast
IAAAM Archive
Frances M.D. Gulland1; Marty Haulena1; Michelle Lander1; Linda J. Lowenstine2; K. Lefebvre3; T. Lipscomb4; T. Rowles5; C. Scholin6; T. Spraker7; V. Trainer8; F. Van Dolah9
1The Marine Mammal Center, Marin Headlands, Sausalito, CA, USA; 2Veterinary Medicine Teaching Hospital, Department Pathology, Microbiology and Immunology, University of California at Davis, CA, USA; 3Institute of Marine Science, University of Santa Cruz, Santa Cruz, CA, USA; 4Armed Forces Institute of Pathology, Veterinary Pathology, Washington, DC, USA; 5National Marine Fisheries Service, Silver Spring, MD, USA; 6Monterey Bay Aquarium Research Institute, Monterey, CA, USA; 7Colorado State University, College of Veterinary Medicine, Fort Collins, CO, USA; 8Marine Biotoxin Group, NOAA/NMFS/ECD, Seattle, WA, USA; 9National Oceanic Services, Charleston, SC, USA

Abstract

Between 15th May and 19th June 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 counties. All animals were in good body 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, the animals showing ataxia and decreased responsiveness to stimuli between seizures and eventually becoming clinically normal. Forty-eight of the 70 animals (67 %) died despite treatment. Of these 70 animals, 54 were adult females, 27 (50 %) of which were pregnant; five were immature females, one was a yearling female, six were subadult males, and four were juvenile males.

Treatment consisted of supportive care with oral and subcutaneous fluids, antibiotic cover with penicillin, control of seizures using diazepam, lorazepam, and phenobarbitone, and reduction of cerebral edema using dexamethasone. Induction of parturition using dexamethasone and prostaglandin F2α was attempted in adult females with open cervices with dead intrauterine fetuses.

Hematological parameters in these stranded sea lions were within normal limits, as were serum biochemical profiles other than creatinine kinase levels. These were elevated in most animals, presumably as a consequence of muscular damage during seizures. Blood lead levels were normal in eight animals and brain cholinesterase normal in five animals tested.

A variety of non-specific lesions were observed on gross post mortem examination. These included gastric ulceration and erosion with associated lymphadenopathy, biliary 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.

The predominant histologic lesion in affected animals was acute neuronal necrosis that was most severe in zones CA3 and CA4 of the hippocampus and the dentate gyri. There were also intramyelinic and neuropil edema and occasional foci of gliosis. In some animals dying within 48 hours of stranding, there was mild multifocal myocardial edema and necrosis.

Domoic acid was detected in serum from three, and urine from a further three affected animals by both a microplate receptor assay method and High Performance Liquid Chromatography (HPLC). It was also detected by HPLC in feces of three of eleven animals tested. Two of these positive fecal samples were examined by scanning electron microscopy, and frustules of Pseudo-nitzschia australis observed.

A bloom of Pseudo-nitzschia australis occurred in Monterey Bay during the later 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 corresponds to the rise and fall of P. australis observed in the plankton. Anchovies collected from the bay on 22nd May 1998 had levels of domoic acid of 105.6 μg domoic acid/g tissue, while fish collected on 10th June 1998 had no detectable levels of domoic acid. Stomachs of anchovies collected during the peak of the P. australis bloom that contained high amounts of domoic acid were also filled with P. australis frustules. In Monterey Bay, the bloom of P. australis was followed by a bloom of P. pseudodelicatissima. Anchovies collected from Monterey Bay reflect this change in species abundance in their stomach contents. No domoic acid was detected in stomachs of these fish or in plankton during the P. pseudodelicatissima bloom.

Three of the 23 sea lions that survived the main "event" in May and June 1998 were equipped with satellite and radio-transmitters prior to release. On 27th November 1998, these three animals were alive; two were within Monterey Bay, and one was diving off San Miguel Island, Channel Islands, central California.

From July 2nd to October 17th 1998, a further 13 California sea lions stranded displaying similar clinical signs to those that stranded in late May and early June. Ten of these stranded between October 3rd and October 17th. Four animals survived, nine died, and these had similar histologic lesions as the earlier cases. Domoic acid was detected in urine of two animals by the microplate assay. At the same time, 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 of Monterey Bay), concentrations of P. australis were in excess of 100,000 cells per liter. It is likely that the source domoic acid affecting sea lions during October originated from a bloom outside of Monterey Bay.

Over the months of May and June 1998, a 3.5 fold increase in numbers of dead beach-cast birds and mammals was detected around the Monterey Bay during routine surveys, than in the same months of the previous year. The majority of the dead birds were common murres, surf scoters and sooty shearwaters.

The combination of clinical signs, histopathological, toxicological, epidemiological and oceanographic changes led to a diagnosis of domoic acid toxicity in the California sea lions.

Domoic acid was first reported as a cause of toxicity in humans in 1987, when four people died and about a hundred were clinically ill following ingestion of contaminated mussels on Prince Edward Island, Canada. This event is the first documented case of domoic acid toxicity in marine mammals.

Speaker Information
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Frances M.D. Gulland, VetMB, PhD, MRCVS
The Marine Mammal Center, Marin Headlands
Sausalito, CA, USA


MAIN : Session IV : Domoic Acid Toxicity
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