Karenia brevis

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Karenia brevis
Karenia brevis.jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Clade: Diaphoretickes
Clade: SAR
Clade: Alveolata
Phylum: Myzozoa
Superclass: Dinoflagellata
Class: Dinophyceae
Order: Gymnodiniales
Family: Kareniaceae
Genus: Karenia
Species:
K. brevis
Binomial name
Karenia brevis
(Davis) G. Hansen et Moestrup

Karenia brevis is a microscopic, single-celled, photosynthetic organism in the genus Karenia . It is a marine dinoflagellate commonly found in the waters of the Gulf of Mexico. [1] It is the organism responsible for the "Florida red tides" that affect the Gulf coasts of Florida and Texas in the U.S., and nearby coasts of Mexico. K. brevis has been known to travel great lengths around the Florida peninsula and as far north as the Carolinas. [2]

Contents

Each cell has two flagella that allow it to move through the water in a spinning motion. K. brevis is unarmored, and does not contain peridinin. Cells are between 20 and 40  μm in diameter. K. brevis naturally produces a suite of potent neurotoxins collectively called brevetoxins, which cause gastrointestinal and neurological problems in other organisms and are responsible for large die-offs of marine organisms and seabirds. [3]

History

The classification of K. brevis has changed over time as advances in technology are made. [4]

Karenia brevis was named for Dr. Karen A. Steidinger [5] in 2001, and was previously known as Gymnodinium breve and Ptychodiscus brevis. It was first named Gymnodinium brevis in 1948, but was later changed to Gymnodinium breve, which correlates with the guidelines of the International Code of Botanical Nomenclature. In 1979 it was categorized under the genus Ptychodiscus and named Ptychodiscus brevis as new research showed it fit better under this genus because of its morphology, biochemistry, and ultrastructure. Then in 1989, scientists agreed this organism should be referred to as its original name (G. breve). It was then reclassified and transferred to the new genus Karenia, which was established at the University of Copenhagen in 2000.

Karenia brevis was first identified in Florida in 1947, but anecdotal reports in the Gulf of Mexico date back to the 1530s. [1] [6] Outbreaks of K. brevis have been known to occur since the Spanish explorers of the 15th and 16th centuries, as documented by Spanish explorers like Cabeza de Vaca.[ citation needed ] These explorers noted large fish kills that resemble the die offs seen in present-day due to K. brevis. C.C. Davis confirmed these die offs were due to K. brevis in 1948. [7]

Ecology and distribution

Karenia brevis has an optimum temperature range of 22–28 °C (72–82 °F), [8] an optimum salinity range of 25-45 Practical Salinity Units (PSU), [9] has adapted to "low-irradiance environments," and can utilize both organic and inorganic nitrogen and phosphorus compounds to survive. [10] In its normal environment, K. brevis will move in the direction of greater light [11] and against the direction of gravity, [12] which will tend to keep the organism at the surface of whatever body of water it is suspended within. The swimming speed of K. brevis is about one metre per hour [13] and the organism can be found throughout the year in the waters of the Gulf of Mexico at concentrations of ≤ 1,000 cell per liter. [2]

Scientists have been unable to determine a definitive geographic range for K. brevis specifically because it is difficult to separate from the ten other species of Karenia, but K. brevis is the most common species occurring in the Gulf of Mexico. [14]

Karenia brevis is the causative agent of red tide, which occurs when the organism multiplies to higher than normal concentrations. During these events the water can take on a reddish or pinkish coloration, giving these explosions in the K. brevis population the name of Florida Red Tide. These algal blooms caused by K. brevis produce brevetoxins, which can result in significant ecological impacts through the death of large numbers of marine animals and birds, to include marine mammals. [15] Large scale fish kills are known to occur due to these Florida Red Tides caused by K. brevis. Fish species through the food chain are impacted, up to and including large predatory species such as sharks, as well as species typical in human consumption. [2]

One researcher has stated that, "There is no single hypothesis that can account for blooms of  K. brevis  along the west coast of Florida". [10] However, like most algae, their occurrence and survival depends on a variety of factors in their environment including water temperature, salinity, light, and nutrients/compounds present in the water. [10] However it is suspected that abundant use of fertilizers in surrounding coastal areas as well as fertilizer run-off from more distant farms, carried by the rivers, might have an impact on algae growth.

Under favorable conditions, toxin-producing dinoflagellates such as K. brevis flourish and grow to high concentrations, an event termed a "harmful algal bloom" or a "HAB". While there are many different types of these HABs and the effects can vary, K. brevis is the causative agent of Florida Red Tides. Due to the toxin that K. brevis produces, these red tides can be detrimental to marine life and can even affect human populations along coasts where they occur. [16]

Impact on human health and activities

In areas where K. brevis is found at normal population levels, the organism is not known to cause harm to human health. It is only at times of unchecked population growth, resulting in harmful algal blooms, when the organism is of concern to human health and activities. [15] The same cannot be said of shellfish harvested and consumed from these algal bloom areas. The brevetoxins released by K. brevis can be found in the flesh of shellfish during Florida Red Tides, potentially causing a condition known as Neurotoxic Shellfish Poisoning (NSP) in humans. Although no recorded human deaths have occurred from NSP, the poisoning does result in nausea, vomiting and a variety of neurological symptoms. [17] Other than NSP, the effects on human health during Florida Red Tide are thought to be limited to respiratory and eye irritation to susceptible persons on the water or close to the shore of areas impacted by the Red Tide, and irritation of skin directly exposed to Florida Red Tide waters. Persons with pre-existing respiratory conditions such as asthma, emphysema or COPD may be more susceptible to harm from the respiratory irritation caused by K. brevis and may be advised to remain away from coastal areas during periods of Florida Red Tide. [15]

The uncontrolled mass explosions of K. brevis populations resulting in Florida Red Tide also has a significant financial impact on the affected coastal areas. The primary source of revenue generation in many of the communities affected by K. brevis red tides is tourism. During periods of red tides this important source of revenue is often lost to the impacted coastal communities of Florida, often on the scale of tens of millions of dollars. [18]

This particular protist is known to be harmful to humans, large fish, and other marine mammals. It has been found that the survival of scleractinian coral is negatively affected by brevetoxin. Scleractinian coral exhibits decreased rates of respiration when there is a high concentration of K. brevis. [3]

Effect of Karenia brevis on Environment

Florida manatee Endangered Florida manatee (Trichechus manatus) (7636816484).jpg
Florida manatee

Brevetoxins are a group of neurotoxic compounds released by K. brevis. At high concentration these brevetoxins can be fatal to fish, marine mammals, and birds. [19] [20] Brevetoxins also pose a threat to corals. [21]

Large nearshore fish fatalities are caused by red-tide blooms. [22] Shorebirds can also get infected with brevetoxins by consuming fish. [23] Thus, red-tide blooms can have major level effects impacting the whole ecosystem. Additionally infected fish and shellfish pose a threat to the fishing industry and economy. [20] [22]

K. brevis red tides have also been found to be a significant factor in the mortality of multiple species of sea turtles. [24] Specifically Kemp's ridleys, loggerheads, green turtles, and hawksbills, particularly along the west Florida coast. [24] Since red tide is a major cause of stranded sea turtles, it contributes to the vulnerability of this endangered species. [24]

K. brevis blooms pose other lethal health risks to marine animals like manatees. Extended occurrences of red tide blooms in the Gulf of Mexico have been associated with substantial instances of mortality in manatee populations [25] . Brevetoxins can lower manatee’s immune systems making them more at risk for other diseases. [25] Additionally, brevetoxin has been correlated with oxidative stress in manatees. [25]

Overall brevetoxins have grave effects on wildlife, and the multitude and compounded effects on entire marine ecosystems are not yet fully understood.

Detection and monitoring

Traditional methods for the detection of K. brevis are based on microscopy or pigment analysis. These are time-consuming, and typically require a skilled microscopist for identification. [26] Cultivation-based identification is extremely difficult and can take several months.

The traditional methods of detection and monitoring of K. brevis blooms from field measurements is labor-intensive and suffers from practical limitations on achieving real-time detection or monitoring. The "Brevebuster" is a deploy-able instrument that can be deployed on automated underwater vehicles or on stationary platforms that can optically detect the Florida red tides. [6] A molecular, real-time PCR-based approach for sensitive and accurate detection of K. brevis cells in marine environments has therefore been developed. [27] A real-time nucleic acid sequence-based amplification (NASBA) assay has been developed for detection of rbcL mRNA from K. brevis. NASBA is sensitive, rapid and effective, and may be used as an additional or alternative method to detect and quantify K. brevis in the marine environment. [28]

Another technique for the detection of K. brevis is multiwavelength spectroscopy, which uses a model-based examination of UV-vis spectra. [29] Methods of detection using satellite spectroscopy have also been developed. [30] [31] Satellite images from Medium Resolution Imaging Spectrometer (MERIS) and Moderate Resolution Imaging Spectroradiometer (MODIS) ocean color sensor, identify K. brevis by making use of its chlorophyll fluorescence and low backscattering characteristics. [32] [33] [34] In addition to methods of detection of cells of K. brevis, enzyme-linked immunosorbent assay (ELISA) and liquid chromatography mass spectrometry (LCMS) have been developed for detecting brevetoxin in shellfish, [6] [35] are more sensitive than the standard mouse bioassay, and as of 2008, were being considered by the Interstate Shellfish Sanitation Conference for regulatory use.

Related Research Articles

<span class="mw-page-title-main">Algal bloom</span> Spread of planktonic algae in water

An algal bloom or algae bloom is a rapid increase or accumulation in the population of algae in freshwater or marine water systems. It is often recognized by the discoloration in the water from the algae's pigments. The term algae encompasses many types of aquatic photosynthetic organisms, both macroscopic multicellular organisms like seaweed and microscopic unicellular organisms like cyanobacteria. Algal bloom commonly refers to the rapid growth of microscopic unicellular algae, not macroscopic algae. An example of a macroscopic algal bloom is a kelp forest.

<i>Gymnodinium</i> Genus of single-celled organisms

Gymnodinium is a genus of dinoflagellates, a type of marine and freshwater plankton. It is one of the few naked dinoflagellates, or species lacking armor known as cellulosic plates. Since 2000, the species which had been considered to be part of Gymnodinium have been divided into several genera, based on the nature of the apical groove and partial LSU rDNA sequence data. Amphidinium was redefined later. Gymnodinium belong to red dinoflagellates that, in concentration, can cause red tides. The red tides produced by some Gymnodinium, such as Gymnodinium catenatum, are toxic and pose risks to marine and human life, including paralytic shellfish poisoning.

<span class="mw-page-title-main">Paralytic shellfish poisoning</span> Syndrome of shellfish poisoning

Paralytic shellfish poisoning (PSP) is one of the four recognized syndromes of shellfish poisoning, which share some common features and are primarily associated with bivalve mollusks. These shellfish are filter feeders and accumulate neurotoxins, chiefly saxitoxin, produced by microscopic algae, such as dinoflagellates, diatoms, and cyanobacteria. Dinoflagellates of the genus Alexandrium are the most numerous and widespread saxitoxin producers and are responsible for PSP blooms in subarctic, temperate, and tropical locations. The majority of toxic blooms have been caused by the morphospecies Alexandrium catenella, Alexandrium tamarense, Gonyaulax catenella and Alexandrium fundyense, which together comprise the A. tamarense species complex. In Asia, PSP is mostly associated with the occurrence of the species Pyrodinium bahamense.

<span class="mw-page-title-main">Thin layers (oceanography)</span> Congregations of plankton

Thin layers are concentrated aggregations of phytoplankton and zooplankton in coastal and offshore waters that are vertically compressed to thicknesses ranging from several centimeters up to a few meters and are horizontally extensive, sometimes for kilometers. Generally, thin layers have three basic criteria: 1) they must be horizontally and temporally persistent; 2) they must not exceed a critical threshold of vertical thickness; and 3) they must exceed a critical threshold of maximum concentration. The precise values for critical thresholds of thin layers has been debated for a long time due to the vast diversity of plankton, instrumentation, and environmental conditions. Thin layers have distinct biological, chemical, optical, and acoustical signatures which are difficult to measure with traditional sampling techniques such as nets and bottles. However, there has been a surge in studies of thin layers within the past two decades due to major advances in technology and instrumentation. Phytoplankton are often measured by optical instruments that can detect fluorescence such as LIDAR, and zooplankton are often measured by acoustic instruments that can detect acoustic backscattering such as ABS. These extraordinary concentrations of plankton have important implications for many aspects of marine ecology, as well as for ocean optics and acoustics. Zooplankton thin layers are often found slightly under phytoplankton layers because many feed on them. Thin layers occur in a wide variety of ocean environments, including estuaries, coastal shelves, fjords, bays, and the open ocean, and they are often associated with some form of vertical structure in the water column, such as pycnoclines, and in zones of reduced flow.

<span class="mw-page-title-main">Brevetoxin</span> Class of chemical compounds produced naturally

Brevetoxin (PbTx), or brevetoxins, are a suite of cyclic polyether compounds produced naturally by a species of dinoflagellate known as Karenia brevis. Brevetoxins are neurotoxins that bind to voltage-gated sodium channels in nerve cells, leading to disruption of normal neurological processes and causing the illness clinically described as neurotoxic shellfish poisoning (NSP).

<span class="mw-page-title-main">Neurotoxic shellfish poisoning</span> Syndrome of shellfish poisoning

Neurotoxic shellfish poisoning (NSP) is caused by the consumption of brevetoxins, which are marine toxins produced by the dinoflagellate Karenia brevis. These toxins can produce a series of gastrointestinal and neurological effects. Outbreaks of NSP commonly take place following harmful algal bloom (HAB) events, commonly referred to as "Florida red tide". Algal blooms are a naturally-occurring phenomenon, however their frequency has been increasing in recent decades at least in-part due to human activities, climate changes, and the eutrophication of marine waters. HABs have been occurring for all of documented history, evidenced by the Native Americans' understanding of the dangers of shellfish consumption during periods of marine bioluminescence. Blooms have been noted to occur as far north as North Carolina and are commonly seen alongside the widespread death of fish and sea birds. In addition to the effects on human health, the economic impact of HAB-associated shellfish toxin outbreaks can have significant economic implications as well due to not only the associated healthcare costs, but the adverse impact on the commercial shellfish industry.

<span class="mw-page-title-main">Harmful algal bloom</span> Population explosion of organisms that can kill marine life

A harmful algal bloom (HAB), or excessive algae growth, is an algal bloom that causes negative impacts to other organisms by production of natural algae-produced toxins, mechanical damage to other organisms, or by other means. HABs are sometimes defined as only those algal blooms that produce toxins, and sometimes as any algal bloom that can result in severely lower oxygen levels in natural waters, killing organisms in marine or fresh waters. Blooms can last from a few days to many months. After the bloom dies, the microbes that decompose the dead algae use up more of the oxygen, generating a "dead zone" which can cause fish die-offs. When these zones cover a large area for an extended period of time, neither fish nor plants are able to survive. Harmful algal blooms in marine environments are often called "red tides".

<i>Karenia</i> (dinoflagellate) Genus of single-celled organisms

Karenia is a genus that consists of unicellular, photosynthetic, planktonic organisms found in marine environments. The genus currently consists of 12 described species. They are best known for their dense toxic algal blooms and red tides that cause considerable ecological and economical damage; some Karenia species cause severe animal mortality. One species, Karenia brevis, is known to cause respiratory distress and neurotoxic shellfish poisoning (NSP) in humans.

<span class="mw-page-title-main">Gymnodiniales</span> Order of single-celled organisms

The Gymnodiniales are an order of dinoflagellates, of the class Dinophyceae. Members of the order are known as gymnodinioid or gymnodinoid. They are athecate, or lacking an armored exterior, and as a result are relatively difficult to study because specimens are easily damaged. Many species are part of the marine plankton and are of interest primarily due to being found in algal blooms. As a group the gymnodinioids have been described as "likely one of the least known groups of the open ocean phytoplankton."

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References

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  11. ↑ Geesey, M. E., and P. A. Tester. 1993. Gymnodinium breveGymnodinium breve: ubiquitous in Gulf of Mexico waters, p. 251-256. InIn T. J. S. Smayda and Shimizu (ed.), Toxic phytoplankton blooms in the sea: Proceedings of the Fifth International Conference on Toxic Marine Phytoplankton. Elsevier Science Publishing, Inc., New York, N.Y.
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  14. ↑ Haywood, Allison J.; Steidinger, Karen A.; Truby, Earnest W.; Bergquist, Patricia R.; Bergquist, Peter L.; Adamson, Janet; Mackenzie, Lincoln (23 January 2004). "Comparative Morphology and Molecular Phylogenetic Analysis of Three New Species of the Genus Karenia (Dinophyceae) from New Zealand1". Journal of Phycology. 40 (1): 165–179. Bibcode:2004JPcgy..40..165H. doi:10.1111/j.0022-3646.2004.02-149.x. ISSN   0022-3646. S2CID   83753181.
  15. 1 2 3 Hoagland, Porter; Jin, Di; Beet, Andrew; Kirkpatrick, Barbara; Reich, Andrew; Ullmann, Steve; Fleming, Lora E.; Kirkpatrick, Gary (July 2014). "The human health effects of Florida Red Tide (FRT) blooms: An expanded analysis". Environment International. 68: 144–153. doi:10.1016/j.envint.2014.03.016. hdl: 1912/6802 . ISSN   0160-4120. PMID   24727069.
  16. ↑ Anderson, Donald M. (August 1997). "Turning back the harmful red tide". Nature. 388 (6642): 513–514. Bibcode:1997Natur.388..513A. doi: 10.1038/41415 . ISSN   0028-0836.
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  18. ↑ Larkin, Sherry L.; Adams, Charles M. (27 August 2007). "Harmful Algal Blooms and Coastal Business: Economic Consequences in Florida". Society & Natural Resources. 20 (9): 849–859. Bibcode:2007SNatR..20..849L. CiteSeerX   10.1.1.513.4469 . doi:10.1080/08941920601171683. ISSN   0894-1920. S2CID   154114902.
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  20. 1 2 Vilas, Daniel; Buszowski, Joe; Sagarese, Skyler; Steenbeek, Jeroen; Siders, Zach; Chagaris, David (13 February 2023). "Evaluating red tide effects on the West Florida Shelf using a spatiotemporal ecosystem modeling framework". Scientific Reports. 13 (1): 2541. doi:10.1038/s41598-023-29327-z. ISSN   2045-2322. PMC   9925760 . PMID   36781942.
  21. ↑ Reynolds, David A.; Yoo, Mi-Jeong; Dixson, Danielle L.; Ross, Cliff (7 February 2020). "Exposure to the Florida red tide dinoflagellate, Karenia brevis, and its associated brevetoxins induces ecophysiological and proteomic alterations in Porites astreoides". PLOS ONE. 15 (2): e0228414. Bibcode:2020PLoSO..1528414R. doi: 10.1371/journal.pone.0228414 . ISSN   1932-6203. PMC   7006924 . PMID   32032360.
  22. 1 2 Gannon, Damon P.; McCabe, Elizabeth J. Berens; Camilleri, Sandra A.; Gannon, Janet G.; Brueggen, Mary K.; Barleycorn, Aaron A.; Palubok, Valeriy I.; Kirkpatrick, Gary J.; Wells, Randall S. (12 March 2009). "Effects of Karenia brevis harmful algal blooms on nearshore fish communities in southwest Florida". Marine Ecology Progress Series. 378: 171–186. Bibcode:2009MEPS..378..171G. doi: 10.3354/meps07853 . ISSN   0171-8630.
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  24. 1 2 3 Foley, Allen M.; Stacy, Brian A.; Schueller, Paul; Flewelling, Leanne J.; Schroeder, Barbara; Minch, Karrie; Fauquier, Deborah A.; Foote, Jerris J.; Manire, Charles A.; Atwood, Karen E.; Granholm, April A.; Landsberg, Jan H. (10 January 2019). "Assessing Karenia brevis red tide as a mortality factor of sea turtles in Florida, USA". Diseases of Aquatic Organisms. 132 (2): 109–124. doi: 10.3354/dao03308 . ISSN   0177-5103. PMID   30628577.
  25. 1 2 3 Walsh, Catherine J.; Butawan, Matthew; Yordy, Jennifer; Ball, Ray; Flewelling, Leanne; de Wit, Martine; Bonde, Robert K. (1 April 2015). "Sublethal red tide toxin exposure in free-ranging manatees (Trichechus manatus) affects the immune system through reduced lymphocyte proliferation responses, inflammation, and oxidative stress". Aquatic Toxicology. 161: 73–84. doi:10.1016/j.aquatox.2015.01.019. ISSN   0166-445X. PMID   25678466.
  26. ↑ Millie, D. F.; Schofield, O. M.; Kirkpatrick, G. J.; Hohnsen, G.; Tester, P. A.; Vinyard, B. T. (1997). "Detection of harmful algal blooms using photopigments and absorption signatures: a case study of the Florida red tide dinoflagellate, Gymnodinium breve. Gymnodinium breve". Limnol. Oceanogr. 42 (5part2): 1240–1251. doi: 10.4319/lo.1997.42.5_part_2.1240 .
  27. ↑ Gray, M.; B. Wawrik; E. Caspar & J.H. Paul (2003). "Molecular Detection and Quantification of the Red Tide Dinoflagellate Karenia brevis in the Marine Environment". Applied and Environmental Microbiology. 69 (9): 5726–5730. Bibcode:2003ApEnM..69.5726G. doi:10.1128/AEM.69.9.5726-5730.2003. PMC   194946 . PMID   12957971.
  28. ↑ Casper, Erica T.; Paul, John H.; Smith, Matthew C.; Gray, Michael (1 August 2004). "Detection and Quantification of the Red Tide Dinoflagellate Karenia brevis by Real-Time Nucleic Acid Sequence-Based Amplification". Appl. Environ. Microbiol. 70 (8): 4727–4732. Bibcode:2004ApEnM..70.4727C. doi:10.1128/AEM.70.8.4727-4732.2004. ISSN   0099-2240. PMC   492458 . PMID   15294808.
  29. ↑ Spear, H. Adam, K. Daly, D. Huffman, and L. Garcia-Rubio. 2009. Progress in developing a new detection method for the harmful algal bloom species, Karenia brevis, through multiwavelength spectroscopy. HARMFUL ALGAE. 8:189–195.
  30. ↑ Hu, C., et al. (2005) Red tide detection and tracing using MODIS fluorescence data: A regional example in SW Florida coastal waters, Remote Sensing of Environment 97(2005) 311–321 http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.115.4645&rep=rep1&type=pdf
  31. ↑ Carvalho, G., et al. (2007) Detection of Florida "red tides" from SeaWiFS and MODIS imagery, Anais XIII Simposio Brasileiro de Sensoriamento Remoto, 21–26 Abril 2007 http://marte.dpi.inpe.br/col/dpi.inpe.br/sbsr@80/2006/11.07.00.35/doc/4581-4588.pdf
  32. ↑ Amin, Ruhul; Zhou, Jing; Gilerson, Alex; Gross, Barry; Moshary, Fred; Ahmed, Samir (25 May 2009). "Novel optical techniques for detecting and classifying toxic dinoflagellate Karenia brevis blooms using satellite imagery". Optics Express. 17 (11): 9126–9144. Bibcode:2009OExpr..17.9126A. doi: 10.1364/OE.17.009126 . ISSN   1094-4087. PMID   19466162.
  33. ↑ Cannizzaro, Jennifer P.; Hu, Chuanmin; English, David C.; Carder, Kendall L.; Heil, Cynthia A.; Müller-Karger, Frank E. (September 2009). "Detection of Karenia brevis blooms on the west Florida shelf using in situ backscattering and fluorescence data". Harmful Algae. 8 (6): 898–909. doi:10.1016/j.hal.2009.05.001. ISSN   1568-9883.
  34. ↑ Soto, Inia M.; Cannizzaro, Jennifer; Muller-Karger, Frank E.; Hu, Chuanmin; Wolny, Jennifer; Goldgof, Dmitry (December 2015). "Evaluation and optimization of remote sensing techniques for detection of Karenia brevis blooms on the West Florida Shelf". Remote Sensing of Environment. 170: 239–254. Bibcode:2015RSEnv.170..239S. doi:10.1016/j.rse.2015.09.026. ISSN   0034-4257.
  35. ↑ Dickey, R. W.; Plakas, S. M.; Jester, E. L.; El Said, K. R.; Johannessen, J. N.; Flewelling, L. J.; Scott, P.; Hammond, D. G.; Van Dolah, F. M.; Leighfield, T. A.; Bottein Dachraoui, M. Y.; Ramsdell, J. S.; Pierce, R. H.; Henry, M. S.; Poli, M. A.; Walker, C.; Kurtz, J.; Naar, J.; Baden, D. G.; Musser, S. M.; White, K. D.; Truman, P.; Miller, A.; Hawryluk, T. P.; Wekell, M. M.; Stirling, D.; Quilliam, M. A.; Lee, J. K. (2004). "Multi-Laboratory Study of Five Methods for the Determination of Brevetoxins in Shellfish Tissue Extracts". Harmful Algae 2002 : Proceedings of the Xth International Conference on Harmful Algae, St. Pete Beach, Florida, USA, October 21-25, 2002. International Conference on Harmful Algae (10th : 2002 : St. Pete Beach, Florida). Vol. 10. pp. 300–302. PMC   4591916 . PMID   26436143.

Glibert, P.M.; Burkholder, J.M (22 May 2014). "The Complex Relationships Between Increases in Fertilization of the Earth, Coastal Eutrophication and Proliferation of Harmful Algal Blooms". Ecology of Harmful Algae. Ecological Studies. Vol. 189. pp. 341–354. doi:10.1007/978-3-540-32210-8_26. ISBN   978-3-540-32209-2.

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