Red tide

A red tide off the coast of La Jolla, San Diego, California.
Red tide in a harbor, Japan

Red tide is a common name for a worldwide phenomenon known as an algae bloom (large concentrations of aquatic microorganisms—protozoans or unicellular algae) when it is caused by species of dinoflagellates and other algae. The upwelling of nutrients from the sea floor from massive storms is most likely the cause of these events.

Overview

Certain species of phytoplankton and dinoflagellates found in red tides contain photosynthetic pigments that vary in color from brown to red. When the algae are present in high concentrations, the water appears to be discolored or murky, varying in color from a rust color to pink to blood red. Specifically, red tide species can be found in oceans, bays, and places where fresh water meets salt water, but they can not thrive in freshwater environments due to the lack of salinity. The growth of the algal bloom depends on wind, temperature, nutrients, and salinity.[1][2] Some red tide algal blooms are associated with fish kills. The production of natural toxins such as brevetoxins[3] and ichthyotoxins are harmful to marine life. Generally, red tides are described as harmful algal blooms. The most conspicuous effects of these kinds of red tides are the associated wildlife mortalities, as well as harmful human exposure.

List of common red tide genera

Harmful toxins produced by the red tide

Marine life exposure

Red tides occur naturally off coasts all over the world. Not all red tides have toxins or are harmful.[4] Where red tides occur, dead fish wash up on shore for up to two weeks after a red tide has been through the area. In addition to killing fish, the toxic algae contaminate shellfish. Some mollusks are not susceptible to the toxin, and store it in their fatty tissues. Shellfish consume the organisms responsible for red tide and concentrate saxitoxin (produced from these organisms) in their tissues. Saxitoxin blocks sodium channels and ingestion can cause paralysis within 30 minutes.[5] Other animals that eat the shellfish are susceptible to the neurotoxin, leading to neurotoxic shellfish poisoning[6] and sometimes even death. Most mollusks and clams filter feed, which results in higher concentrations of the toxin than just drinking the water.[7] Scaup, for example, are diving ducks whose diet mainly consists of mollusks. When scaup eat the filter-feeding shellfish that are concentrated with high levels of the red tide toxin, their population along with other types of diving ducks become a prime target for poisoning. However, even birds that do not eat mollusks can be affected by simply eating dead fish on the beach or drinking the water, as in the Peking duck experiment.[8] The toxins released by the blooms can kill marine animals including dolphins, sea turtles, birds, and manatees.[9][10] Marine dinoflagellates produce ichthyotoxins. Fish such as Atlantic herring, American pollock, winter flounder, Atlantic salmon, and cod were dosed orally with these toxins in an experiment. Within minutes of receiving doses of the toxin, fish started to exhibit a loss of equilibrium and began to swim in an irregular, jerking pattern followed by paralysis and shallow, arrhythmic breathing and eventually death after about an hour.[11] Scientists concluded that the toxic red tide had negative effects on fish that were exposed to it.

Human exposure

Humans are affected by the red tide species by ingesting improperly harvested shellfish, breathing in aerosolized brevetoxins (i.e. PbTx or Ptychodiscus toxins) and in some cases skin contact. The brevetoxins bind to voltage-gated sodium channels, important structures of cell membranes. Binding results in persistent activation of nerve cells, which interferes with neural transmission leading to health problems. These toxins are created within the unicellular organism, or as a metabolic product.[12] The two major types of brevetoxin compounds have similar but distinct backbone structures. PbTx-2 is the primary intracellular brevetoxin produced by K. brevis blooms. However, over time, the PbTx-2 brevetoxin can be converted to PbTx-3 through metabolic changes.[12] Researchers found that PbTx-2 has been the primary intracellular brevetoxin that converts overtime into PbTx-3.[13] When the cells rupture, they release extracellular brevetoxins into the environment. Some of those stay in the ocean, while other particles get aerosolized. During onshore winds, brevetoxins can become aerosolized by bubble-mediated transport, causing respiratory irritation, bronchoconstriction, coughing, and wheezing among other symptoms.[14] On a windy day, avoiding contact with the aerosolized toxin is recommended. These individuals report a decrease in respiratory function after only 1 hour of exposure to a K. brevis red-tide beach and these symptoms may last for days.[15] People with severe or persistent respiratory conditions (such as chronic lung disease or asthma) may experience stronger adverse reactions. The National Oceanic and Atmospheric Administration's National Ocean Service provides a public conditions report identifying possible respiratory irritation impacts in areas affected by red tides.[16]

In most cases like in the U.S., the seafood consumed by humans is tested regularly for toxins by the USDA to ensure safe consumption. However, improper harvesting of shellfish can cause paralytic shellfish poisoning and neurotoxic shellfish Poisoning in humans. Some symptoms include drowsiness, diarrhea, nausea, loss of motor control, tingling, numbing or aching of extremities, incoherence, and respiratory paralysis.[17] Lastly, reports of skin irritation after swimming in the ocean during a red tide are common, so people should try to avoid the red tide when it is in the area.

Red tide

The dinoflagellate labeled above is the microscopic alga Karenia brevis. It is the cause of red tide in the Gulf of Mexico. The algae propel themselves using a longitudinal flagellum (A) and a transverse flagellum (B). The longitudinal flagellum lies in a groove-like structure called the cingulum (F). The dinoflagellate is separated into an upper portion called the epitheca (C) where the apical horn resides (E) and a lower portion called the hypotheca (D).

Red tide is a colloquial term used to refer to one of a variety of natural phenomena known as harmful algal blooms. The term specifically refers to blooms of a species of dinoflagellate.[18] It is being phased out among researchers because:

  1. Red tides are not necessarily red and many have no discoloration at all.
  2. They are unrelated to movements of the tides.
  3. The term is imprecisely used to refer to a wide variety of algal species that are known as bloom-formers.

As a technical term, it is being replaced in favor of more precise terminology, including the generic term "harmful algal bloom" for harmful species, and "algal bloom" for benign species.

On the U.S. coasts

The term red tide is most often used in the US to refer to Karenia brevis blooms in the eastern Gulf of Mexico, also called the Florida red tide. K. brevis is one of many different species of the genus Karenia found in the world's oceans. [19] Major advances have occurred in the study of dinoflagellates and their genomics. Some include identification of the toxin-producing genes (PKS genes), exploration of environmental changes (temperature, light/dark, etc.) have on gene expression, as well as an appreciation of the complexity of the Karenia genome.[19] These blooms have been documented since the 1800s, and occur almost annually along Florida's coasts.[19] There was increased research activity of HABs in the 1980s and 1990s. This was primarily driven by media attention from the discovery of new HAB organisms and the potential adverse health effects of their exposure to animals and humans.[20] The Florida red tides have been observed to have spread as far as the eastern coast of Mexico.[19] The density of these organisms during a bloom can exceed tens of millions of cells per litre of seawater, and often discolor the water a deep reddish-brown hue.

Red tide is also sometimes used to describe harmful algal blooms on the northeast coast of the United States, particularly in the Gulf of Maine. This type of bloom is caused by another species of dinoflagellate known as Alexandrium fundyense. These blooms of organisms cause severe disruptions in fisheries of these waters, as the toxins in these organism cause filter-feeding shellfish in affected waters to become poisonous for human consumption due to saxitoxin.[21] The related Alexandrium monilatum is found in subtropical or tropical shallow seas and estuaries in the western Atlantic Ocean, the Caribbean Sea, the Gulf of Mexico, and the eastern Pacific Ocean.

Factors that may contribute to a bloom

Red tide (NOAA)

Red tides contain dense concentrations of organisms and appear as discolored water, often reddish-brown in color. It is a natural phenomenon, but the exact cause or combination of factors that result in a red tide outbreak are not necessarily known.[22] However, three key factors are thought to play an important role in a bloom - salinity, temperature, and wind. Red tides cause economic harm, so outbreaks are carefully monitored. For example, the Florida Fish and Wildlife Conservation Commission provides an up-to-date status report on red tides in Florida.[23] The Texas Parks and Wildlife Department also provides a status report.[24] While no particular cause of red tides has been found, many different factors can contribute to their presence. These factors can include water pollution, which originates from sources such as human sewage and agricultural runoff.[25]

The occurrence of red tides in some locations appears to be entirely natural (algal blooms are a seasonal occurrence resulting from coastal upwelling, a natural result of the movement of certain ocean currents)[26][27] while in others they appear to be a result of increased nutrient pollution from human activities.[28] The growth of marine phytoplankton is generally limited by the availability of nitrates and phosphates, which can be abundant in agricultural run-off as well as coastal upwelling zones. Coastal water pollution produced by humans and systematic increase in seawater temperature have also been implicated as contributing factors in red tides. Other factors such as iron-rich dust influx from large desert areas such as the Sahara Desert are thought to play a major role in causing red tides.[29] Some algal blooms on the Pacific Coast have also been linked to occurrences of large-scale climatic oscillations such as El Niño events. While red tides in the Gulf of Mexico have been occurring since the time of early explorers such as Cabeza de Vaca,[30] what initiates these blooms and how large a role anthropogenic and natural factors play in their development is unclear. Whether the apparent increase in frequency and severity of algal blooms in various parts of the world is in fact a real increase or is due to increased observation effort and advances in species identification methods is also debated.[31][32]

Increasing temperature, enhanced surface stratification, alteration of ocean currents, intensification or weakening of local nutrient upwelling, stimulation of photosynthesis by elevated CO2, reduced calcification through ocean acidification, and heavy precipitation and storm events causing changes in land runoff and micronutrient availability may all produce contradictory species- or even strain-specific responses.[33] In terms of harmful algal blooms (HABs), we can expect: (i) range expansion of warm-water species at the expense of cold-water species, which are driven poleward; (ii) species-specific changes in the abundance and seasonal window of growth of HAB taxa; (iii) earlier timing of peak production of some phytoplankton; and (iv) secondary effects for marine food webs, notably when individual zooplankton and fish grazers are differentially impacted by climate change.[33] However, the potential consequences of these changes for HABs have received relatively little attention and are not well understood. Substantial research is needed to evaluate the direct and indirect associations between HABs, climate change, ocean acidification, and human health.[34]

A multi-partner project funded by the federal EcoHab program (NOAA) and published by the Mote Marine Laboratory shows a list of what feeds red tides.[35] A study from the Florida FWC shows the Karenia brevis algae red tide found in Florida is fed and worsened by nitrogen (N) and phosphorus (P).[36]

Notable occurrences

  • 1530: First alleged case off the Florida Gulf Coast is without foundation.[37] According to Marine Lab at University of Miami, the first Red Tide in Florida was in 1844. Earlier "signs" were from boats sorting fish on their way to home port dumping trash fish overboard. Thus "dead fish" reports along the coast were not Red Tide.[38]
  • 1793: The first recorded case occurring in British Columbia, Canada.[39]
  • 1840: No deaths of humans have been attributed to Florida red tide, but people may experience respiratory irritation (coughing, sneezing, and tearing) when the red tide organism (Karenia brevis) is present along a coast and winds blow its aerosolized toxins. Swimming is usually safe, but skin irritation and burning is possible in areas of high concentration of red tide.[40]
  • 1844: First verified case off the Florida Gulf Coast according to Marine Lab University of Miami, probably by ships off shore, no known inhabitants of the coast reporting.[41]
  • 1916: Massive fish kill along SW Florida coast. Noxious air thought to be seismic underwater explosion releasing chlorine gas.[42]
  • 1947: Southwest Florida
  • 1972: A red tide was caused in New England by a toxic dinoflagellate Alexandrium (Gonyaulax) tamarense. The red tides caused by the dinoflagellate Gonyaulax are serious because this organism produces saxitoxin and gonyautoxins which accumulate in shellfish and if ingested may lead to paralytic shellfish poisoning (PSP) and can lead to death.[43]
  • 1972 and 1973: Red tides killed two villagers west of Port Moresby. In March 1973 a red tide invaded Port Moresby Harbour and destroyed a Japanese pearl farm.[44]
  • 1976: The first PSP case in Sabah, Malaysian Borneo where 202 victims were reported to be suffering and 7 deaths.[39][45][46]
  • 2005: The Canadian red tide was discovered to have come further south than it has in years prior by the ship (R/V) Oceanus,[47] closing shellfish beds in Maine and Massachusetts and alerting authorities as far south as Montauk (Long Island, NY) to check their beds.[48] Experts who discovered the reproductive cysts in the seabed warn of a possible spread to Long Island in the future, halting the area's fishing and shellfish industry and threatening the tourist trade, which constitutes a significant portion of the island's economy.
  • 2005-2006: Southwest Florida Karenia brevis
  • 2011: Northern California[49]
  • 2011: Gulf of Mexico[50]
  • 2013: On January, a red tide occurred again on the West Coast Sea of Sabah in the Malaysian Borneo.[45][51] Two human fatalities were reported after they consumed shellfish contaminated with the red tide toxin.[45][46][51]
  • 2013: January, a red tide bloom appeared at Sarasota beach – mainly Siesta Key, Florida causing a fish kill that had a negative impact on tourists, and caused respiratory issues for beach-goers.[52]
  • 2014: August, massive 'Florida red tide' 90 miles long and 60 miles wide.[53]
  • 2015: June, 12 persons hospitalized in the Philippine province of Bohol for red tide poisoning.[54]
  • 2015: August, several beaches in the Netherlands between Katwijk and Scheveningen were plagued. Government institutions dissuaded swimmers from entering the water.[55]
  • 2015: September, a red tide bloom occurred in the Gulf of Mexico, affecting Padre Island National Seashore along North Padre Island and South Padre Island in Texas.[56]
  • 2016: September, Texas Parks and Wildlife report red tide in the Lower Laguna Madre. "High to moderate concentrations of red tide have been found from Beach Access 6 to the Brazos Santiago jetties. Moderate cell concentrations have been found at the Isla Blanca Park boat ramp."[57]
  • 2017 and 2018: K. brevis red tide algae with warnings not to swim, state of emergency declared, dead dolphin and manatee, worsened by Caloosahatchee River. Toxic harmful algae bloom red tide in Southwest Florida.[58][59][60]A rare harmful algal bloom along Florida’s east coast of Palm Beach County occurred the weekend of September 30th, 2018.[61]

See also

References

  1. ↑ Alcock, Frank. "An Assessment of Florida red tide: Causes, Consequences and Management Strategies." 2007. 6 March 2018.
  2. ↑ "Discover NOAA's Coral Reef Data". www8.nos.noaa.gov. Archived from the original on 2012-07-26. Retrieved 2009-08-22.
  3. ↑ http://www.nmfs.noaa.gov/pr/pdfs/health/brevetoxin.pdf
  4. ↑ Gregg W. Langlois, Pamela D. Tom. "Red Tides: Questions and Answers". U.S. Government. Retrieved 2009-08-23.
  5. ↑ "Red Tide FAQ – Is it safe to eat oysters during a red tide?". www.tpwd.state.tx.us. Retrieved 2009-08-23.
  6. ↑ Watkins, Sharon M.; Reich, Andrew; Fleming, Lora E.; Hammond, Roberta (2008). "Neurotoxic Shellfish Poisoning". Marine Drugs. 6 (3): 431–455. doi:10.3390/md20080021. PMC 2579735. PMID 19005578.
  7. ↑ Brand et al., Larry E., Lisa Campbell, Eileen Bresnan. "Karenia: The biology and ecology of a toxic genus." Harmful Algae 14 (2012): 156–178. 6 March 2018.
  8. ↑ Forrester et al., Donald J., Jack M. Gaskin, Franklin H. White. "AN EPIZOOTIC OF WATERFOWL IN FLORIDA." Journal of Wildlife Diseases 13 (1997): 160–167.
  9. ↑ "Red Tide & Red Algae Effects". 2015.
  10. ↑ "Top 10 Red Tide Facts" (PDF). Florida Department of Health. 2016.
  11. ↑ White, A. W. "Sensitivity of Marine Fishes to Toxins from the Red-Tide Dinoflagellate Gonyaulax excavata and Implications for Fish Kills." Marine Biology 65 (1981): 255–260. 6 March 2018.
  12. 1 2 Pierce, R. H., & Henry, M. S. (2008). Harmful algal toxins of the Florida red tide (Karenia Brevis): natural chemical stressors in South Florida coastal ecosystems. Ecotoxicology (London, England), 17(7), 623–631. doi:10.1007/s10646-008-0241-x.
  13. ↑ Pierce, R.H., M. S. Henry. "Harmful algal toxins of the Florida red tide (Karenia brevis): natural chemical stressors in South Florida coastal ecosystems." Ecotoxicology (2008): 623–631. 6 March 2018.
  14. ↑ Backer et al., Lorraine C., Laura E. Flemming, Alan Rowan. "Recreational exposure to aerosolized brevetoxins during Florida red tide events." Harmful Algae 2 (2003): 19–28. 6 March 2018.
  15. ↑ Fleming LE, Kirkpatrick B, Backer LC, et al. Initial evaluation of the effects of aerosolized Florida red tide toxins (brevetoxins) in persons with asthma. Environ Health Perspect. 2005;113:650–657.
  16. ↑ "Harmful Algal Bloom Operational Forecast System". www.tidesandcurrents.noaa.gov/hab/. Retrieved 2012-02-14.
  17. ↑ Van Dolah, Frances M. "Marine Algal Toxins: Origins, Health Effects, and Their Increased Occurrence." Environmental Health Perspectives 108 (2000): 133–141. 6 March 2018. PMC 1637787.
  18. ↑ "Harmful Algal Blooms (HABs): Red Tide". U.S. Centers for Disease Control and Prevention. Retrieved 2 Oct 2011.
  19. 1 2 3 4 Fleming, L.E.; Kirkpatrick, B.; Backer, L.C.; Walsh, C.J.; Nierenberg, K.; Clark, J.; et al. (2011). "Review of Florida red tide and human health effects". Harmful Algae. Elsevier. 10 (2): 224–233. doi:10.1016/j.hal.2010.08.006.
  20. ↑ Abraham and Baden, 2006; Backer et al., 2003a, 2005a; Backer and Fleming, 2008; Fleming et al., 2001; Fleming et al., 2004; Okamoto and Fleming, 2005; Twiner et al., 2008; Zaias et al., 2010.
  21. ↑ "Red Tide (Paralytic Shellfish Poisoning)" (PDF). Boston, MA: Massachusetts Department of Public Health. 2015.
  22. ↑ "Red Tide FAQ". Austin, TX: Texas Parks and Wildlife Department. Retrieved 2018-08-15.
  23. ↑ "Red Tide Current Status Statewide Information". Florida Fish and Wildlife Research Institute. Archived from the original on 2009-08-22. Retrieved 2009-08-23.
  24. ↑ "Red Tide Index". Texas Parks and Wildlife Department. Retrieved 2018-08-15.
  25. ↑ West, L. (2016). "Red Tide: Causes and Effects". About News.
  26. ↑ Trainer, VL; Adams, NG; Bill, BD; Stehr, CM; Wekell, JC; Moeller, P; Busman, M; Woodruff, D (2000). "Domoic acid production near California coastal upwelling zones, June (1998)". Limnol Oceanogr. 45: 1818–1833. Bibcode:2000LimOc..45.1818T. doi:10.4319/lo.2000.45.8.1818.
  27. ↑ Adams, NG; Lesoing, M; Trainer, VL (2000). "Environmental conditions associated with domoic acid in razor clams on the Washington coast". J Shellfish Res. 19: 1007–1015.
  28. ↑ Lam CWY, Ho KC (1989) Red tides in Tolo Harbor, Hong Kong. In: Okaichi T, Anderson DM, Nemoto T (eds) Red tides. Biology, environmental science and toxicology. Elsevier, New York, pp 49–52.
  29. ↑ Walsh; et al. (2006). "Red tides in the Gulf of Mexico: Where, when, and why?". Journal of Geophysical Research. 111: C11003. Bibcode:2006JGRC..11111003W. doi:10.1029/2004JC002813. PMC 2856968.
  30. ↑ Cabeza de Vaca, Álvar Núnez. La Relación (1542). Translated by Martin A. dunsworth and José B. Fernández. Arte Público Press, Houston, Texas (1993)
  31. ↑ Sellner, K.G.; Doucette G.J.; Kirkpatrick G.J. (2003). "Harmful Algal blooms: causes, impacts and detection". Journal of Industrial Microbiology and Biotechnology. 30 (7): 383–406. doi:10.1007/s10295-003-0074-9. PMID 12898390.
  32. ↑ Van Dolah, F.M. (2000). "Marine Algal Toxins: Origins, Health Effects, and Their Increased Occurrence". Environmental Health Perspectives. 108 (suppl.1): 133–141. doi:10.2307/3454638. JSTOR 3454638. PMC 1637787. PMID 10698729. Archived from the original on 2009-01-20.
  33. 1 2 Hallegraeff, Gustaaf M. (2010-04-01). "Ocean, Phytoplankton Community Responses, and Harmful Algal Blooms: A Formidable Predictive Challenge1". Journal of Phycology. 46 (2): 220–235. doi:10.1111/j.1529-8817.2010.00815.x. ISSN 1529-8817.
  34. ↑ Moore, Stephanie K.; Trainer, Vera L.; Mantua, Nathan J.; Parker, Micaela S.; Laws, Edward A.; Backer, Lorraine C .; Fleming, Lora E. (2008-01-01). "Impacts of climate variability and future climate change on harmful algal blooms and human health". Environmental Health. 7 (2): S4. doi:10.1186/1476-069X-7-S2-S4. ISSN 1476-069X. PMC 2586717. PMID 19025675.
  35. ↑ "Nutrients That Feed Red Tide "Under the Microscope" in Major Study". News & Press. Sarasota, FL: Mote Marine Laboratory. Retrieved 2018-07-05.
  36. ↑ "What forms of nutrients can Karenia brevis use to grow and bloom?". HAB Research. Tallahassee, FL: Florida Fish and Wildlife Conservation Commission. Retrieved 2018-08-15.
  37. ↑ A historical assessment of Karenia brevis in the western Gulf of Mexico (PDF), 2018-08-16
  38. ↑ "Log In or Sign Up to View" (PDF). lookaside.fbsbx.com. Retrieved 2018-07-21.
  39. 1 2 "PARALYTIC SHELLFISH POISONING (PSP)". Sabah Fish Department.com. Retrieved 2013-01-11.
  40. ↑ "Marine & Natural Resources – Red Tide & Fish Kill Resources – Taylor County Extension Office". Retrieved 18 October 2016.
  41. ↑ "Log In or Sign Up to View" (PDF). lookaside.fbsbx.com. Retrieved 2018-07-21.
  42. ↑ "Punta Gorda Herald, Dec. 7 1916".
  43. ↑ HAB 2000 Archived 2008-12-11 at the Wayback Machine.
  44. ↑ MacLean, J.L. (February 1974). "Shellfish Poisoning in the South Pacific" (PDF). South Pacific Commission.
  45. 1 2 3 "Red tide warning". New Straits Times. 2013-01-06. Archived from the original on 2013-01-07. Retrieved 2013-01-07.
  46. 1 2 "2 Red Tide deaths in Sabah". Daily Express. 2013-01-06. Retrieved 2013-01-11.
  47. ↑ "R/V Oceanus Archived Information". Retrieved 18 October 2016.
  48. ↑ Moore, Kirk. "Northeast Oysters: The bigger danger, growers assert, would be the label of endangered". National Fisherman. Archived from the original on 2007-08-08. Retrieved 2008-07-31.
  49. ↑ Fimrite, Peter (2011-09-17). "Red tide killing abalone off California". The San Francisco Chronicle.
  50. ↑ "Texas Gulf Coast Sees Largest Algae Bloom in Over A Decade". Huffington Post. 2011-10-18.
  51. 1 2 MUGUNTAN VANAR (2013-01-07). "Sabah issues red tide alert". The Star Online. Archived from the original on 2013-01-08. Retrieved 2013-01-07.
  52. ↑ McSwane, J. David. "UPDATE: Red tide, fish kill reported at Sarasota beaches". Retrieved 18 October 2016.
  53. ↑ Netburn, Deborah (11 August 2014). "Massive 'Florida red tide' is now 90 miles long and 60 miles wide". Orlando Sentinel. Retrieved 30 September 2015.
  54. ↑ Israel, Dale G. (June 25, 2015). "12 persons hospitalized in Bohol for red tide poisoning".
  55. ↑ "Rijkswaterstaat, do not swim between Katwijk and Scheveningen". Dutch Public Broadcasting, NOS. 3 August 2015. Retrieved 30 September 2015.
  56. ↑ "Red Tide in Texas, Current Status". Texas Parks and Wildlife. 15 September 2015. Retrieved 30 September 2015.
  57. ↑ Nora Salinas. "Red tide arrives at South Padre Island".
  58. ↑ "Algae, red tide impacting SWFL water quality". WINK NEWS. 2018-07-04. Retrieved 2018-07-05.
  59. ↑ Glenn, Julie. "Toxic Algae Blooms, Red Tide, and the Need for a Permanent Solution". Retrieved 2018-07-05.
  60. ↑ "What forms of nutrients can Karenia brevis use to grow and bloom?". myfwc.com. Retrieved 2018-08-14.
  61. ↑ https://www.miamiherald.com/news/article219331165.html
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