Harmful algal blooms Topic 4

Learning goals To understand classification and biological sources of harmful algal blooms To learn biological mechanisms of action of algal toxins Practical implications: prediction, prevention and control

What are HABs? Algae that produce toxins  Dinoflagellates  Diatoms  Cyanobacteria (fresh water) Very potent toxins (few cells per liter can produce toxic effects) Adversely affect overall environmental quality

Environmental impacts Toxic effects on organisms Physical impairment of fish Nuisance conditions from odors or discoloration of water or habitats

History of HABs HABs are not a new phenomenon! Documentation of HABs goes back to ancient times Apparent increase of the HAB occurrence in modern times – real or imaginary?

HABs in US: Pre- and post-1972

“Red” Tide World-wide occurrence Algae:  Dinoflagellates  Diatoms

“Brown” Tide World-wide occurrence Algae  Chrysophyta (“golden- brown algae”) Aureococcus Aureoumbra

Toxic dinoflagellate blooms  Ciguatera Fish Poisoning  Diarrhetic Shellfish Poisoning  Neurotoxic Shellfish Poisoning  Paralytic Shellfish Poisoning Toxic diatom blooms  Amnesic Shellfish Poisoning Harmful blooms (non-toxic or toxicity not confirmed)  Fish kills Pfiesteria, Chaetoceros, Heterosigma  Brown tides Aureococcus, Aureoumbra Algae associated with HABs

Ciguatera Fish Poisoning Gambierdiscus toxicus (a dinoflagellate) Associated with weeds and coral reefs Optimum conditions: shallow waters, °C, ppt Ciguatoxin and maitotoxin

Ciguatera Fish Poisoning Ciguatoxin

Mechanism of action Selective activation of voltage-sensitive Na + channels

Ciguatera Fish Poisoning

Mechanism of action Selectively activates voltage dependent calcium channels

Ciguatera Fish Poisoning Common cause of food-borne poisoning ~ 50% of US seafood poisoning  90% - Florida and Hawaii  Spring/Summer

Ciguatera Fish Poisoning: Vectors Usually large fish, bottom dwellers and reef fish  Red snapper, Grouper, Amber Jack, Sturgeon Toxins  Bioaccumulate  Stable and heat resistant  Lipid soluble  Highly potent (clinical effects from <1 mg)

Lag time <12 h Acute onset Early symptoms (24-48 h): Gastrointestinal  Pain, cramping, diarrhea, vomiting Late symptoms  Neurological Headache, toothache Temperature disturbance (hot-cold sensation reversal) Respiratory paralysis and seizure in severe cases  Cardiovascular Heart rate abnormalities (rare), usually bradycardia Ciguatera Fish Poisoning: Symptoms in humans

Ciguatera Fish Poisoning: Treatment and prevention Diagnosis  Biomarkers of exposure not available Therapy  Not available Prevention  Complicated Wide range of susceptible species Odorless, colorless, tasteless Avoidance  Large reef fish  Avoiding roe, head, viscera

Diarrhetic Shellfish Poisoning Dinoflagellates  Dinophysis acuminata, Dinophysis fortii, Prorocentrum lima Species reported in the US but associated illnesses not reported Okadaic acids and dinophysistoxins

Diarrhetic Shellfish Poisoning

Mechanisms of action Inhibits phosphatase 1 and 2A which control Na + secretion from intestinal cells Loss of fluids and ions from gut epithelial cells

Diarrhetic Shellfish Poisoning: Human Symptoms Generally mild gastrointestinal illness  Diarrhea, nausea, vomiting  Rapid onset, rapid resolution  No neurotoxic effects  Long-term effects? (Possibly tumorigenic) FDA level in shellfish – 0.2 ppm okadaic acid plus 35-methyl-okadaic acid

Neurotoxic Shellfish Poisoning Karenia brevis (previously Gymnodinium breve) Florida, Gulf of Mexico Brevetoxins

Neurotoxic Shellfish Poisoning

Mechanism of action Selective activation of voltage-sensitive Na + channels

Neurotoxic Shellfish Poisoning: Human Symptoms Similar to ciguatera poisoning Early symptoms: Gastrointestinal  Nausea, diarrhea, vomiting Late symptoms  Neurological Tingling Numbness Loss of motor control Usually not associated with human mortality FDA level in fish – 0.8 ppm brevitoxin-2 equivalent

Brevetoxins: Ecological Impacts Massive fish kills Harmful to birds (pelican, seagulls, cormorants) and manatees

Brevetoxins: Economical Impacts Human health-associated impacts Closure of shellfish beds Skin and respiratory irritation to humans at the seashore Losses in commercial catch and tourism

Paralytic Shellfish Poisoning Dinoflagellates  Alexandrium spp.  Gymnodinium spp.  Pyrodinium spp. Northern Atlantic and Pacific coasts Temperate and tropical Saxitoxins

Paralytic Shellfish Poisoning

Mechanism of action Binds and blocks voltage-dependent sodium channels Blocks neuron activity and affects peripheral nervous system

Paralytic Shellfish Poisoning: Human Symptoms Rapid onset (~30 min) Absence of gastrointestinal symptoms Neurological symptoms  Numbness  Headache  Ataxia  Weakness  Cranial nerve dysfunction  Diaphragmatic paralysis  Death by asphyxiation Weakness can persist for weeks

Paralytic Shellfish Poisoning: Therapy and Prevention Therapy  Not available (supportive only) FDA limit in fish 0.8 ppm

Saxitoxins: Ecological Impacts Mass bivalve mortality ( ,000,000 mussels, 1980; ,000, Eland Bay, South Africa) Lobster mortality (Eland Bay, South Africa) Humpback whales (Cape Cod, MA) 1997 South Africa

Amnesic Shellfish Poisoning Pseudo-nitzschia spp. (diatoms) Discovered in 1987 (Price Edward Isl., Canada) Domoic acid

Amnesic Shellfish Poisoning Domoic Acid Glutamic acid

Mechanisms of action Mimics a neurotransmitter (glutamic acid) Overstimulates and eventually kills neurons in hypocampus Stimulates voltage- dependent calcium channels

Amnesic Shellfish Poisoning: Human Symptoms Early symptoms: Gastrointestinal  Nausea, vomiting, diarrhea CNS symptoms  Dizziness  Cognitive effects  Disorientation  Memory loss  Delirium  Seizures  Agitation Highly variable course  10% with permanent neurological damage

Domoic acid: Ecological Effects 1991 Monterey Bay CA - >100 pelicans and cormorants were found dead or suffering from unusual neurological symptoms Pseudo-nitzschia australis Vector: Northern Anchovie

Pfiesteria piscicida: fish kills Unknown substances secreted by finfish and shellfish stimulate Pfiesteria to transform from benthic cysts or amoebae or non- toxic flagellated cells, to toxic zoospores

Pfiesteria in humans Rare  Narcosis  Sores  Nausea/vomiting  Acute short-term memory loss  Severe cognitive impairment Recovery in 6-8 weeks, but may re-occur Most cases – Chesapeake fishermen and algal researchers (aerosol!)

HABs: Distribution in the US

HABs: What can we do about it? Prevention  Complicated  Public awareness (=negative publicity for fish and shellfish industry) Prediction  Satellite tracking of red and brown tides  Mathematical models predicting blooms

Satellite images: Karenia brevis in NC, 1987

Staellite images: Red tide in FL, 1978