Red tides and marine mammal mortalities

Flewelling, Leanne J.; Naar, Jérôme; Abbott, Jay P.; Baden, Daniel G.; Barros, Nélio B.; Bossart, Gregory D.; Bottein, Marie‐Yasmine Dechraoui; Hammond, Daniel G.; Haubold, Elsa M.; Heil, Cynthia A.; Henry, Michael S.; Jacocks, Henry M.; Leighfield, Tod A.; Pierce, Richard H.; Pitchford, Thomas D.; Rommel, Sentiel A.; Scott, Paula S.; Steidinger, Karen A.; Truby, Earnest W.; Dolah, Frances M. Van; Landsberg, Jan H.

doi:10.1038/nature435755a

Cited by 360 publications

(294 citation statements)

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“…Brevetoxins can lead to human health concerns through the consumption of shellfish contaminated by accumulated brevetoxins, known as neurological shellfish poisoning, or through reduced respiratory function from aerosolized brevetoxins in sea spray (1,3,4). In addition, K. brevis blooms have led to massive fish kills and compromise sea turtle, sea bird, and marine mammal health, playing a major role in the ecology of the Gulf of Mexico (1,5).…”

mentioning

confidence: 99%

Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis

Errera¹,

Campbell

2011

Proc. Natl. Acad. Sci. U.S.A.

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With the increase in frequency of harmful algal blooms (HABs) worldwide, a better understanding of the mechanisms that influence toxin production is needed. Karenia brevis , the major HAB dinoflagellate in the Gulf of Mexico, produces potent neurotoxins, known as brevetoxins. Human health is directly impacted by blooms of K. brevis through consumption of shellfish contaminated by accumulated brevetoxins (neurotoxic shellfish poisoning) or from aerosolized brevetoxins in sea spray (reduced respiratory function); however, the reason for brevetoxin production has remained a mystery. Here we show that brevetoxin production increased dramatically in response to osmotic stress in three of the four K. brevis clones examined. By rapidly changing salinity to simulate a shift from oceanic conditions to a decreased salinity typical of coastal conditions, brevetoxin production was triggered. As a result, brevetoxin cell quota increased by >14-fold, while growth rate remained unchanged. Live images of K. brevis cells were also examined to assess changes in cell volume. In the K. brevis Wilson clone, cells responded quickly to hypoosmotic stress by increasing their brevetoxin cell quota from ∼10 to 160 pg of brevetoxin per cell, while cell volume remained stable. In contrast, the K. brevis SP1 clone, which has a consistently low brevetoxin cell quota (<1 pg per cell), was unable to balance the hypoosmotic stress, and although brevetoxin production remained low, average cell volume increased. Our findings close a critical gap in knowledge regarding mechanisms for toxin production in K. brevis by providing an explanation for toxin production in this harmful dinoflagellate.

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mentioning

confidence: 99%

Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis

Errera¹,

Campbell

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…In humans, brevetoxins cause neurotoxic shellfish poisoning, and brevetoxin-contaminated aerosols cause respiratory irritation and illness (2, 5). Blooms also cause massive fish kills (6), as well as bird and marine mammal mortalities (7,8). In 2005, a bloom of K. brevis lasted for more than a year and caused extensive mortalities at all trophic levels in lagoons, coastal ecosystems, and offshore reefs on the west Florida shelf (8, 9).…”

mentioning

confidence: 99%

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

Sunda

Burleson

Hardison

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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With the global proliferation of toxic harmful algal bloom species, there is a need to identify the environmental and biological factors that regulate toxin production. One such species, Karenia brevis, forms nearly annual blooms that threaten coastal regions throughout the Gulf of Mexico. This dinoflagellate produces brevetoxins, which are potent neurotoxins that cause neurotoxic shellfish poisoning and respiratory illness in humans, as well as massive fish kills. A recent publication reported that a rapid decrease in salinity increased cellular toxin quotas in K. brevis and hypothesized that brevetoxins serve a role in osmoregulation. This finding implied that salinity shifts could significantly alter the toxic effects of blooms. We repeated the original experiments separately in three different laboratories and found no evidence for increased brevetoxin production in response to low-salinity stress in any of the eight K. brevis strains we tested, including three used in the original study. Thus, we find no support for an osmoregulatory function of brevetoxins. The original publication also stated that there was no known cellular function for brevetoxins. However, there is increasing evidence that brevetoxins promote survival of the dinoflagellates by deterring grazing by zooplankton. Whether they have other as-yet-unidentified cellular functions is currently unknown. red tides | toxic blooms | HABs H armful algal blooms threaten human health and damage coastal ecosystems worldwide. In the Gulf of Mexico, the athecate dinoflagellate Karenia brevis causes nearly annual toxic blooms. The physiology, ecology, and adverse effects of K. brevis have been well studied since the species was described in the 1940s (1). Notably, K. brevis produces brevetoxins, a family of potent polyether neurotoxins that bind to voltage-activated sodium channels in cell membranes, preventing normal nerve and muscle activity (2, 3). A nontoxic polyether that inhibits brevetoxin function, brevenal, is also produced in small amounts by this species (4). In humans, brevetoxins cause neurotoxic shellfish poisoning, and brevetoxin-contaminated aerosols cause respiratory irritation and illness (2, 5). Blooms also cause massive fish kills (6), as well as bird and marine mammal mortalities (7,8). In 2005, a bloom of K. brevis lasted for more than a year and caused extensive mortalities at all trophic levels in lagoons, coastal ecosystems, and offshore reefs on the west Florida shelf (8, 9).Because of the extensive damage caused by K. brevis, there has been considerable interest in understanding the function and regulation of brevetoxins. Competition experiments reveal that K. brevis produces allelopathic compounds, which inhibit the growth of competing phytoplankton and thereby help enable this slowgrowing species to dominate; however, brevetoxins themselves do not appear to be responsible for this inhibition (10, 11). Recent studies support the hypothesis that brevetoxins serve as grazing deterrents, which promote population survival by decrea...

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“…In theory, even human mortalities could result from neurotoxic shellfish poisoning (NSP), although no mortalities have yet been linked conclusively to this source (Fleming et al 2011). FRTassociated mortalities have been observed in marine mammals, however, including manatees and oceanic dolphins, and also in sea turtles, seabirds, and finfish (Flewelling et al 2005, Landsberg et al 2009, Fire and Van Dolah 2012, Capper et al 2013.…”

Section: Introductionmentioning

confidence: 99%

“…Kirkpatrick et al (2010) found ED visits for digestive illnesses at the Sarasota Memorial Hospital increased by 40% during an FRT bloom event in 2001 (0.07 ± 0.01 per 100,000 cases) relative to 2002 (0.05 ± 0.01 per 100,000 cases) when there was no FRT bloom. Although shellfish harvest areas (SHAs) typically were closed during FRT blooms to mitigate the risks of NSP from the consumption of molluscan bivalves, these authors argued that humans could be contracting digestive illnesses through other pathways, including the consumption of illegally harvested shellfish, whole finfish (especially the entrails, where brevetoxins may be concentrated), the breathing of aerosols contaminated with brevetoxins, or the inadvertent swallowing of contaminated seawater (Flewelling et al 2005). …”

Section: Introductionmentioning

confidence: 99%

The human health effects of Florida Red Tide (FRT) blooms: An expanded analysis

Hoagland

Jin

Beet

et al. 2014

Environment International

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Abstract:Human respiratory and digestive illnesses can be caused by exposures to brevetoxins from blooms of the marine alga Karenia brevis, also known as Florida red tide (FRT). K. brevis requires macro-nutrients to grow; although the sources of these nutrients have not been resolved completely, they are thought to originate both naturally and anthropogenically. The latter sources comprise atmospheric depositions, industrial effluents, land runoffs, or submerged groundwater discharges. To date, there has been only limited research on the extent of human health risks and economic impacts due to FRT. We hypothesized that FRT blooms were associated with increases in the numbers of emergency room visits and hospital inpatient admissions for both respiratory and digestive illnesses. We sought to estimate these relationships and to calculate the costs of associated adverse health impacts. We developed environmental exposure-response models to test the effects of FRT blooms on human health, using data from diverse sources. We estimated the FRT bloom-associated illness costs, using extant data and parameters from the literature.When controlling for resident population, a proxy for tourism, and seasonal and annual effects, we found that increases in respiratory and digestive illnesses can be explained by FRT blooms.Specifically, FRT blooms were associated with human health and economic effects in older cohorts (≥ 55 years of age) in six southwest Florida counties. Annual costs of illness ranged from $60,000 to $700,000 annually, but these costs could exceed $1.0 million per year for severe, long-lasting FRT blooms, such as the one that occurred during 2005. Assuming that the average annual illness costs of FRT blooms persist into the future, using a discount rate of 3%, the capitalized costs of future illnesses would range between $2-24 million.3

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Red tides and marine mammal mortalities

Cited by 360 publications

References 5 publications

Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis

Osmotic stress triggers toxin production by the dinoflagellate Karenia brevis

Osmotic stress does not trigger brevetoxin production in the dinoflagellateKarenia brevis

The human health effects of Florida Red Tide (FRT) blooms: An expanded analysis

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