Potentially Toxic or Harmful Microalgae from the Northeast Coast Paul E. Hargraves; Lucie Maranda Northeastern Naturalist, Vol. 9, No. 1. (2002), pp. 81-120. Stable URL: http://links.jstor.org/sici?sici=1092-6194%282002%299%3A1%3C81%3APTOHMF%3E2.0.CO%3B2-C Northeastern Naturalist is currently published by Humboldt Field Research Institute.
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NORTHEASTERN NATURALIST
9(1):81-120
POTENTIALLY TOXIC OR HARMFUL
MICROALGAE FROM THE NORTHEAST COAST
ABSTRACT - We have described the occurrence of 46 phytoplankton species that are potentially toxic to humans, or harmful to marine life, or both. The area of interest is southeastern Nova Scotia to the Hudson River (NY) estuary. The species are distributed across a number of taxonomic classes. and represent a conservative estimate of the real total, which must remain speculative until the biodiversity of phytoplankton in the area is known. Despite the high number of potential harmful algal bloom (HAB) species,rather few are known to cause problems.
INTRODUCTION It is often speculated that the first recorded harmful algal bloom is biblical (Exodus 7:20-21) and records an event several thousand years old. More recently, there is general acceptance that the occurrence of harmful algal blooms (HABs) is increasing on a worldwide scale (Anderson et al. 2000, Hallegraeff 1993). In part this may be due to increased public awareness and expansion of mariculture or sea-farming, leading to a higher level of observation (Hallegraeff 1993). Also, modification of the coastal environment by human activity appears to have increased the likelihood that various planktonic and benthic microalgae are becoming a threat to human health and fisheries resources (Anderson et al. 2000, Hallegraeff 1995). Yet many visible growths of microalgae are completely innocuous or even beneficial; conversely, many harmful outbreaks have no visible manifestation at all. The rapid expansion of mariculture may itself be a contributing cause to harmful algal outbreaks through local nutrient enrichment of enclosed waters. and by confinement of animals to conditions which may become inimical (Hallegraeff 1995). The annual loss from HABs worldwide is probably over $1 billion, including both mortality and unmarketable products; the annual human cost has been estimated as 2000 cases of poisoning with 15% mortality (Hallegraeff 1995). Because there is no international record of economic loss and human intoxication incidents by HABs. these numbers are almost certainly underestimates. Microalgal species causing HABs can be grouped in three major categories: those causing illness or death in humans; those causing illness or death in marine life through direct chemical or physical interference with metabolic activity: and those causing marine mortality
' Graduate School of Oceanography. University of Rhode Island, Narragansett, RI 02882-1 197:
[email protected].
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secondarily, resulting from anoxia or sulfide intoxication as blooms decay naturally. We eliminate the third category from consideration here since virtually any species, if abundant, can cause localized anoxia leading to marine mortality. Also excluded are allelopathic interactions (when a species may chemically inhibit potential conipetitors). In this discussion we consider all microalgal species as phytoplankton (itself a colloquial term), although a few are primarily benthic and are found adventitiously in the plankton. Thus included are species with known toxin profiles, species suspected of producing toxins with undetermined characteristics, species causing physical harm or damage. and species causing impairment to biological functions of marine organisms. Species causing human illness are frequently considered according to the nature of their toxicity (Anderson et al. 1998. Hallegraeff et al. 1995). These phytoplankters produce toxins that find their way through the food chain to humans, causing a variety of gastrointestinal and neurological illness . Details on the epidemiology of these illnesses and chemistry of the toxins and their analogs are available in a number of places: in print (e.g., Anderson et al. 1998, Hallegraeff 1993, Hallegraeff et a1.1995 [second edition now in prep.]. Reguera et al. 1998, Shilnizu 1996, Yasumoto et al. 1996) and available on many websites (e.g., http:// vm.cfsan.fda.ov/-mow/chap37.html:
www.rsmas.miami.edu/groups/ niehs; www.redtide.whoi.edu/hab/illness/illnesshtml. In this work we present only a brief summary. Most cases corresponding to these syndromes result from eating contaminated shellfish or fish. Amnesic shellfish poisoning (ASP) is primarily caused by domoic acid produced by diatoms: outbreaks are known from Atlantic Canada and the U.S. west coast, but the causative species occur worldwide (Hallegraeff et al. 1995. Hasle et al. 1996). Domoic acid is a small molecular-weight amino acid with water-soluble properties. It binds to glutamate receptors in the brain and central nervous system, thus acting as a neurotoxin. and some fatalities have occurred (Hallegraeff et al. 1995: see the Bates bibliography at website http://dfomr.mar.dfompo.gc.ca/science/mesd/he/toxins/da.html).
Ciguatera fish poisoning (CFP or ciguatera) is primarily confined to the tropics (Anderson et al. 2000, Hallegraeff et al. 1995), but some dinoflagellates producing these toxins are found in the northeast (see below). Ciguatera results from the action of a suite of toxins. The two most common are ciguatoxin and maitotoxin, both high molecularweight structures of linked polyether rings. Ciguatera produces gastrointestinal, cardiovascular, and neurological disturbance following ingestion of toxin-laden fish, but is generally not fatal, although symptoms can persist for months (Anderson et al. 1998, Hallegraeff 1995; website http://\lm.cfsan.fda.gov/-mow/chap36.html). Diarrhetic shellfish poisoning (DSP) is caused by a group of linear polyether toxins, including lipid-soluble okadaic acid and its many de-
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rivatives. Okadaic acid strongly inhibits protein phosphatase activity (Quillam and Wright 1995), is nonfatal but carcinogenic. and is associated with severe gastrointestinal distress (Hallegraeff et al. 1995, website http://www.rsmas.miami.edu/groups/niehs/health/toxintable.html). The chemically related yessotoxins have been grouped with DSP but have different toxicological properties (Yasumoto and Satake 1998). Neurotoxic shellfish poisoning (NSP) is most common in the Gulf of Mexico but some dinoflagellates that produce the associated gastrointestinal and neurological disturbances (usually nonfatal) occur elsewhere (Hallegraeff 1995, website http://www.floridamarine.org). The brevetoxins implicated in NSP are frequently dispersed as aerosols, thus causing eye and nose irritation, but they can also accumulate in shellfish (Hallegraeff 1995). These lipid-soluble polyether rings bind to sodium channels in cell membranes and impair neuromuscular functions (Wright and Cembella 1998). The most severe human illness in the northeast is paralytic shellfish poisoning (PSP), a life-threatening illness caused by a potent group of neurotoxins (Hallegraeff et al. 1995, website http:// www.rsmas.miami.edu/groups/niehs/health/toxintable.html) There are over 20 of these tetrahydropurines known as saxitoxins (Shimizu 1996) that act by blocking sodium channels in cell membranes. In severe cases, ingestion of toxic shellfish can lead to ~nuscularparalysis and asphyxiation. The existence of PSP has been recognized for centuries (Brongersma-Sanders 1957, Vancouver 1798). In addition to the above. cyanobacteria can produce chemicals which cause intense skin irritation and gastroenteritis when ingested (Christoffersen 1996, Sivonen 1996) but have yet to acquire an acronym, perhaps due to their rarity of harmful occurrence in marine coastal environments. Phytoplankters causing illness and mortality in marine life encompass a much broader group of toxins and syndromes and are much less studied. For convenience they can be grouped into those producing one or more chemicals directly affecting respiration, reproduction, feeding. and other physiological processes; and those affecting life processes by physical or mechanical means such as gill clogging. We emphasize that species causing human illness frequently cause marine mortality or inhibition as well (Rensel1995. Turner and Tester1 997) and some species affect marine life by a combination of chemical and physical irritants (Burkholder 1998, Shumway 1990). Research on these topics is advancing rapidly. The actual number of events of proven toxicity to humans in the northeast is quite small (Anderson et al. 2000). Events causing harm to marine life are undoubtedly more common, but often undetected or unreported. Starting points for summaries of toxicity and mortality are the papers by Burkholder (1998). Richardson (1997), Shumway (1990), the early but mostly unrecognized summary of Brongersma-Sanders (1957).
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and the websites mentioned above. Specific research topics concerning HAB species and toxin chemistry are found in the biennial proceedings of harmful algae conferences (e.g., Reguera et al. 1998, Yasumoto et al. 1996). The coastal waters of the northeastern U.S. and adjacent Canadian maritime provinces are home to a very large number of phytoplankton species. The exact number of specie? is unknown because, unfortunately, the biodiversity has never been adequately documented. We conservatively estimate that the total is 500 different species, but the real number may well be closer to 1000. Of these it appears that about 10% are potentially harmful. Because the occurrence of these potentially toxic and harmful species has not been summarized previously for this part of northeastern North America. we have done so.
METHODS For the purpose of geographic limitation we define "northeast" as the area from the southeast coast of Nova Scotia to the Hudson River estuary in New York and out to the edge of the continental shelf. This area has some oceanographic uniformity and economically is the major part of the Northeast LME (Large Marine Ecosystem; Sherman et a1.1996). The species included are primarily those we have seen ourselves, but we have also relied on literature records of occurrences. Unfortunately these records are always subject to some scepticism because of the variability in taxonomic expertise of various identifiers; generally we have been optimistic that identifications have been accurate. Also included are records of strains isolated from the northeast available at the Provasoli-Guillard National Center for Culture of Marine Phytoplankton (hereafter called CCMP, at website: http://ccmp.bigelow.org/). Each species is accompanied by one or more illustrations, with dimensional summary in Table 1. These are intended to show the general appearance and characteristics of the species, and are not intended as authoritative identification aids. For this, access to a variety of published manuals is necessary. A good starting point for critical identification is the volume edited by Tomas ( 1997). The species are presented alphabetically within taxonomic classes. The species we have included in this list are considered potentially toxic to humans in the northeast if at least one of the following conditions applies: 1) one or more strains of the species is known to produce toxins affecting humans (ASP. DSP, PSP, etc.); 2 ) the species is strongly implicated or proven to cause human illness or fatality; or 3) the species has produced a positive reaction in mammalian toxicity tests (e.g., mouse bioassay). We have considered species harmful to marine life if one or both of the following conditions apply: 1) one or more strains are known to produce metabolites harmful or detrimental to normal life processes; or 2) the species is strongly implicated or proven to cause mortality under laboratory or natural conditions.
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Table 1. Dimensions of individual cells of species with toxic a ~ ~ d i harmful or effects; measurements in pm, unless otherwise indicated. Measurements of species in this work may differ from other literature records (p. a.: pervalvar axis, d.: diameter, a. a.: apical axis. t. a.: transapical axis). References are: I, Balech (1995); 2, Taylor et al. (1995): 3. Hasle and Syvertsen (1997); 4. Throndsen (1997); 5. Dodge (1982): 6, summarizedin this work.
DINOPHYCEAE A1e;candrirrm ander.soni Alexandrrum fundyense Alexandrium rninutlrm Ale.zandrium ostenfeldii Alexandririm tamurense Amphidinium carrerae Ceratium fusus Cochlodinium polykrikoides Coolia monori~ Dinophysic ucuminatrr Dinophysi, acura Dinophysis currdutn Dinoph.v~i.sjortii Dinophyii~norvegica Dinophysis tripor G?mnodinirrm mikimotoi G?mnodininnz sanguineum Lingulodinium polyedrrcm Phalacromu rotundarum Prorocentrum lima Prorocentrirm nlrnimurn Proroceratiurn rrriculatrrm Scrippsiella rrochoiden BACILLARIOPHYCEAE Cerataulina pelagica Chaeroreror conca~'icornis Chaeroceros debilis Coscinodiscus centralis Cuscinodircu~conrinnus Coscrnodiscus wailrsii Pielrdohm~antidiumpacific~im Pseudo-nrrzschia delicatissima Pserrdo-rrirzsihia jraudulentu Pseudo-nitzschia rnultiseries Preudo-nitzrchia pseudodelicatissima Pserrdo-nrr,-schia pungens seriatu P~eud
