Mixotrophic dinoflagellate

Last updated

Dinoflagellata
Temporal range: 250–0  Ma
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Triassic or earlier–Present
Britannica Dinoflagellata 2.jpg
Illustrations of various Dinoflagellata
Scientific classification
Domain:
Eukaryota
(unranked):
SAR
(unranked):
Alveolata
Phylum:
Dinoflagellata

Bütschli 1885 [1880-1889] sensu Gomez 2012 [1] [2] [3]
Classes
Synonyms
  • Cilioflagellata Claparède & Lachmann, 1868
  • Dinophyta Dillon, 1963
  • Dinophyceae sensu Pascher, 1914
  • Pyrrophyta Pascher 1914
  • Pyrrhophycophyta Papenfuss 1946
  • Arthrodelen Flagellaten Stein 1883
  • Dinomastigota Margulis & Sagan, 1985
  • Dinophyta Dillon, 1963

Dinoflagellates are eukaryotic plankton, existing in marine and freshwater environments. Previously, dinoflagellates had been grouped into two categories, phagotrophs and phototrophs. [4] Mixotrophs, however include a combination of phagotrophy and phototrophy. [5] Mixotrophic dinoflagellates are a sub-type of planktonic dinoflagellates and are part of the phylum Dinoflagellata. [5] They are flagellated eukaryotes that combine photoautotrophy when light is available, and heterotrophy via phagocytosis. Dinoflagellates are one of the most diverse and numerous species of phytoplankton, second to diatoms.

Contents

Dinoflagellates have long whip-like structures called flagella that allow them to move freely throughout the water column. They are mainly marine but can also be found in freshwater environments. Combinations of phototrophy and phagotrophy allow organisms to supplement their inorganic nutrient uptake [6] This means an increased trophic transfer to higher levels in food web compared to the traditional food web. [6]

Mixotrophic dinoflagellates have the ability to thrive in changing ocean environments, resulting in shifts in red tide phenomenon and paralytic shellfish poisoning. [6] It is unknown as to how many species of dinoflagellates have mixotrophic capabilities, as this is a relatively new feeding-mechanism discovery.

Species

Some dinoflagellates that live as parasites are probably mixotrophic. [7] Karenia , Karlodinium , and Lepidodinium are some of the dinoflagellate genera which are thought to contain peridinin, a carotenoid pigment necessary for photosynthesis in dinoflagellates; [8] however, chlorophyll b has been found in these genera as an accessory pigment. [8] This discovery has led scientists to assume that the pigment chlorophyll b actually came from prey which had been ingested by the dinoflagellates. [8] Some species of mixotrophic dinoflagellate are able to feed on toxic prey such as toxic algae and other toxic organisms. For example, Lingulodinium polyedra and Akashiwo sanguinea are two species of mixotrophic dinoflagellates that are known to feed on the toxic dinoflagellate, Alexandrium tamarense . [9] Certain species of mixotrophic dinoflagellates can be affected by light intensity and nutrient conditions . For example, ingestion rates of Fragilidium subglobosum, Gymnodinium gracilentum, and Karlodinium veneficum increase as light intensity increases up to 75 to 100 μmol photons per m2 per second. [10] In contrast, other species are not affected by light intensity. [10] As well, ingestion rates of the mixotrophic dinoflagellate Ceratium furca are affected by intracellular nutrient concentrations. [11]

Types of feeding

Marine dinoflagellate species undergo three major trophic modes: autotrophy, mixotrophy and heterotrophy. [12] Many species of dinoflagellates were previously assumed to be exclusively autotrophic; however, recent research has revealed that many dinoflagellates that were thought to be exclusively phototrophic are actually mixotrophic. [12] Mixotrophic dinoflagellates can undergo both photosynthesis and phagocytosis as methods of feeding. [7] Mixotrophic dinoflagellates with individual plastids that depend mostly on photosynthesis can prey on other cells as their secondary source of nutrients. [7] On the other hand, mixotrophic dinoflagellates with individual plastids that depend mainly on phagocytosis are also photosynthetic due to chloroplasts 'stolen' from their prey (kleptochloroplasts) or because of algal endosymbionts. [7] It was discovered that the mixotrophic dinoflagellates Gonyaulax polygramma and Scrippsiella spp. can engulf small-size prey using their apical horn while larger prey are engulfed via their sulcus, showing that dinoflagellates can have more than one mouth for feeding. [9] Moreover, mixotrophic dinoflagellates belonging to the species Karlodinium armiger, can capture small prey by direct engulfment or can use an extendable peduncle to capture larger prey. [13]

Implications for microbial food webs

Mixotroph dinoflagellates belonging to the species Gymnodinium sanguineum feed on nanociliate populations in Chesapeake Bay. [14] Predation on ciliates is advantageous for G. sanguineum as the ciliates provide a source of nitrogen which is limiting to the growth of purely photosynthetic dinoflagellates. [14] By preying on ciliates, these dinoflagellates reverse the normal flow of material from primary producer to consumer and influence the trophodynamics of the microbial food web in Chesapeake Bay [14]

Several established ecological models of marine microbial food webs have not included feeding by mixotrophic dinoflagellates. [12] These additions would include feeding by mixotrophic dinoflagellates on bacteria, phytoplankton, other mixotrophic dinoflagellates and nanoflagellates, and heterotrophic protists. [12] The impact of grazing by mixotrophic dinoflagellates will affect particular prey species and be influenced by the abundance of dinoflagellate predators and their ingestion rates. [12] Another consideration would be to include predator-prey relationships of mixotrophic dinoflagellates at a species level due to co-existence in offshore and oceanic waters. [12]

The diversity of mixotrophic dinoflagellate species and their interactions with other marine organisms contributes to their diverse roles in different niche environments. [12] For example, mixotrophic and heterotrophic dinoflagellates may act as predators on a wide range of prey types due to their diverse feeding mechanisms. [12] Including mixotrophic dinoflagellates would better explain the control of prey population and cycling of limited materials as well as competition between other organisms for larger prey. [12]

Climate Change and Ocean Acidification

As CO2 concentrations in the atmosphere increase via anthropogenic causes, acidification of the ocean will increase as the result of increasing CO2 sequestration by the ocean; the ocean is a great sink for carbon, absorbing more as its concentration in the atmosphere increases. [15] As this occurs, there will be species and community composition shifts in marine plankton communities. Mixotrophic dinoflagellates will be favoured over photosynthetic dinoflagellates, as the oceans will become more nutrient limited and mixotrophs will not have to rely only on inorganic nutrients but will be able to take advantage of being able to consume particulate organic matter. [6]

With an increase in temperature, there is an increase in water column stability, [15] which leads to favourable conditions for mixotrophic growth. Mixotrophs can grow in low nutrient (more stable) environments and become dominant members of planktonic communities. [6] Harmful algal blooms (HABs) can be caused by increased stability or increases in nutrients due to acidification and climate change, as well. This can have large impacts on the food chain and pose harmful effects to humans and their food sources [6] through harmful blooms of dinoflagellates and other taxa, and lead to paralytic shellfish poisoning, for example. [16]

Influence on red tide and HABs

Algal bloom (akasio) by Noctiluca spp. in Nagasaki Algal bloom(akasio) by Noctiluca in Nagasaki.jpg
Algal bloom (akasio) by Noctiluca spp. in Nagasaki

Many mixotrophic and some heterotrophic dinoflagellates are known to cause red tides or harmful blooms that result in large-scale mortality of fish and shellfish. [12] Studies on red tides have been conducted to determine the mechanism of outbreak and the persistence of red tides caused by mixotrophic dinoflagellates such as Karenia brevis , Prorocentrum donghaiense and Prorocentrum minimum in low nutrient concentration waters. In the case of serial red tides, one mixotrophic dinoflagellate species is dominated by another mixotrophic species in rapid succession over a short span of days. [12] A possible explanation for the occurrence of different dominant mixotrophic dinoflagellates during serial red tides is the ability of mixotrophic dinoflagellates to feed on both heterotrophic bacteria and cyanobacteria (such as Synecchococcus ) spp., which provide limiting nutrients such as phosphorus, and nitrogen simultaneously. [12] It is proposed that during serial red tides, feeding by larger mixotrophic dinoflagellates on smaller species may be a driving force for the succession of dominant species. [12] Nitrogen and phosphorus is taken up by direct transfer of the materials and energy between the mixotrophic dinoflagellates; therefore, nutrient supply does not rely on the release of nitrogen and phosphorus by other organisms. Hence, mixotrophy can cause uncoupling between nutrient concentrations and the abundance of mixotrophic dinoflagellates in natural environments. [12]

Red tides are a type of harmful algal bloom (HABs); both are the result of massive proliferation of algae that result in very high concentrations of cells that visibly colour the water. [17] The very high levels of biomass in Red Tides or HABs can have direct toxic effects through the release of toxic compounds or indirect effects through oxygen depletion on mammals, fish, shellfish, and humans. [17] PSP (Paralytic Shellfish Poisoning) is one example of a toxin that is produced by dinoflagellates that can have lethal consequences if contaminated shellfish are ingested; the toxin is a neuro-inhibitor that is concentrated in the flesh of bivalves and molluscs that have fed on toxic algae [18] The toxin concentrations can cause harmful and even deadly effects on humans and marine mammal populations that feed on contaminated shellfish. [18]

Relationship to other organisms

Mixotrophic dinoflagellates can feed on various organisms including bacteria, picoeukaryotes, nanoflagellates, diatoms, protists, metazoans and other dinoflagellates, as well. [8] Feeding and digestion rates in mixotrophic dinoflagellates are lower than those in strictly heterotrophic dinoflagellates. [8] Mixotrophic dinoflagellates do not feed on blood, eggs, adult metazoans, and flesh, such as occurs in some heterotrophic dinoflagellates.

Related Research Articles

<span class="mw-page-title-main">Plankton</span> Organisms living in water or air that are drifters on the current or wind

Plankton are the diverse collection of organisms that drift in water but are unable to actively propel themselves against currents. The individual organisms constituting plankton are called plankters. In the ocean, they provide a crucial source of food to many small and large aquatic organisms, such as bivalves, fish, and baleen whales.

<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.

<span class="mw-page-title-main">Zooplankton</span> Heterotrophic protistan or metazoan members of the plankton ecosystem

Zooplankton are the animal component of the planktonic community, having to consume other organisms to thrive. Plankton are aquatic organisms that are unable to swim effectively against currents. Consequently, they drift or are carried along by currents in the ocean, or by currents in seas, lakes or rivers.

<span class="mw-page-title-main">Dinoflagellate</span> Unicellular algae with two flagella

The dinoflagellates are a monophyletic group of single-celled eukaryotes constituting the phylum Dinoflagellata and are usually considered protists. Dinoflagellates are mostly marine plankton, but they also are common in freshwater habitats. Their populations vary with sea surface temperature, salinity, and depth. Many dinoflagellates are photosynthetic, but a large fraction of these are in fact mixotrophic, combining photosynthesis with ingestion of prey.

<i>Noctiluca scintillans</i> Bioluminescent, marine dinoflagellate

Noctiluca scintillans is a marine species of dinoflagellate that can exist in a green or red form, depending on the pigmentation in its vacuoles. It can be found worldwide, but its geographical distribution varies depending on whether it is green or red. This unicellular microorganism is known for its ability to bioluminesce, giving the water a bright blue glow seen at night. However, blooms of this species can be responsible for environmental hazards, such as toxic red tides. They may also be an indicator of anthropogenic eutrophication.

<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.

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

The genus Ceratium is restricted to a small number of freshwater dinoflagellate species. Previously the genus contained also a large number of marine dinoflagellate species. However, these marine species have now been assigned to a new genus called Tripos. Ceratium dinoflagellates are characterized by their armored plates, two flagella, and horns. They are found worldwide and are of concern due to their blooms.

<span class="mw-page-title-main">Predatory dinoflagellate</span>

Predatory dinoflagellates are predatory heterotrophic or mixotrophic alveolates that derive some or most of their nutrients from digesting other organisms. About one half of dinoflagellates lack photosynthetic pigments and specialize in consuming other eukaryotic cells, and even photosynthetic forms are often predatory.

<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.

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

Oxyrrhis is a genus of heterotrophic dinoflagellate, the only genus in the family Oxyrrhinaceae. It inhabits a range of marine environments worldwide and is important in the food web dynamics of these ecosystems. It has the potential to be considered a model organism for the study of other protists. Oxyrrhis is an early-branching lineage and has long been described in literature as a monospecific genus, containing only Oxyrrhis marina. Some recent molecular phylogenetic studies argue that Oxyrrhis comprises O. marina and O. maritima as distinct species, while other publications state that the two are genetically diverse lineages of the same species. The genus has previously been suggested to contain O. parasitica as a separate species, however the current consensus appears to exclude this, with Oxyrrhis being monospecific and containing O. marina and O. maritima as separate lineages of the type species. The genus is characterised by its elongated body which is anteriorly prolonged to a point, its complex flagellar apparatuses which attach to the ventral side of the cell, and the unique features of its nucleus.

A mixotroph is an organism that can use a mix of different sources of energy and carbon, instead of having a single trophic mode on the continuum from complete autotrophy at one end to heterotrophy at the other. It is estimated that mixotrophs comprise more than half of all microscopic plankton. There are two types of eukaryotic mixotrophs: those with their own chloroplasts, and those with endosymbionts—and those that acquire them through kleptoplasty or through symbiotic associations with prey or enslavement of their organelles.

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

Alexandrium is a genus of dinoflagellates. It contains some of the dinoflagellate species most harmful to humans, because it produces toxic harmful algal blooms (HAB) that cause paralytic shellfish poisoning (PSP) in humans. There are about 30 species of Alexandrium that form a clade, defined primarily on morphological characters in their thecal plates.

Alexandrium catenella is a species of dinoflagellates. It is among the group of Alexandrium species that produce toxins that cause paralytic shellfish poisoning, and is a cause of red tide. Alexandrium catenella is observed in cold, coastal waters, generally at temperate latitudes. These organisms have been found in the west coast of North America, Japan, Australia, and parts of South Africa.

<i>Oxyrrhis marina</i> Species of single-celled organism

Oxyrrhis marina is a species of heterotrophic dinoflagellate with flagella that is widely distributed in the world's oceans.

<i>Cochlodinium polykrikoides</i> Species of single-celled organism

Cochlodinium polykrikoides is a species of red tide producing marine dinoflagellates known for causing fish kills around the world, and well known for fish kills in marine waters of Southeast Asia. C. polykrikoides has a wide geographic range, including North America, Central America, Western India, Southwestern Europe and Eastern Asia. Single cells of this species are ovoidal in shape, 30-50μm in length and 25-30μm in width.

<i>Dinophysis acuminata</i> Species of dinoflagellate

Dinophysis acuminata is a marine plankton species of dinoflagellates that is found in coastal waters of the north Atlantic and Pacific oceans. The genus Dinophysis includes both phototrophic and heterotrophic species. D. acuminata is one of several phototrophic species of Dinophysis classed as toxic, as they produce okadaic acid which can cause diarrhetic shellfish poisoning (DSP). Okadiac acid is taken up by shellfish and has been found in the soft tissue of mussels and the liver of flounder species. When contaminated animals are consumed, they cause severe diarrhoea. D. acuminata blooms are constant threat to and indication of diarrhoeatic shellfish poisoning outbreaks.

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

Polykrikos is one of the genera of family Polykrikaceae that includes athecate pseudocolony-forming dinoflagellates. Polykrikos are characterized by a sophisticated ballistic apparatus, named the nematocyst-taeniocyst complex, which allows species to prey on a variety of organisms. Polykrikos have been found to regulate algal blooms as they feed on toxic dinoflagellates. However, there is also some data available on Polykrikos being toxic to fish.

<span class="mw-page-title-main">Marine protists</span> Protists that live in saltwater or brackish water

Marine protists are defined by their habitat as protists that live in marine environments, that is, in the saltwater of seas or oceans or the brackish water of coastal estuaries. Life originated as marine single-celled prokaryotes and later evolved into more complex eukaryotes. Eukaryotes are the more developed life forms known as plants, animals, fungi and protists. Protists are the eukaryotes that cannot be classified as plants, fungi or animals. They are mostly single-celled and microscopic. The term protist came into use historically as a term of convenience for eukaryotes that cannot be strictly classified as plants, animals or fungi. They are not a part of modern cladistics because they are paraphyletic.

Lepidodinium is a genus of dinoflagellates belonging to the family Gymnodiniaceae. Lepidodinium is a genus of green dinoflagellates in the family Gymnodiniales. It contains two different species, Lepidodiniumchlorophorum and Lepidodinium viride. They are characterised by their green colour caused by a plastid derived from Pedinophyceae, a green algae group. This plastid has retained chlorophyll a and b, which is significant because it differs from the chlorophyll a and c usually observed in dinoflagellate peridinin plastids. They are the only known dinoflagellate genus to possess plastids derived from green algae. Lepidodinium chlorophorum is known to cause sea blooms, partially off the coast of France, which has dramatic ecological and economic consequences. Lepidodinium produces some of the highest volumes of Transparent Exopolymer Particles of any phytoplankton, which can contribute to bivalve death and the creation of anoxic conditions in blooms, as well as playing an important role in carbon cycling in the ocean.

References

  1. ↑ Gómez F (2012). "A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata)". CICIMAR Oceánides. 27 (1): 65–140. doi: 10.37543/oceanides.v27i1.111 .
  2. ↑ Ruggiero; et al. (2015), "Higher Level Classification of All Living Organisms", PLOS ONE, 10 (4): e0119248, doi: 10.1371/journal.pone.0119248 , PMC   4418965 , PMID   25923521
  3. ↑ Silar, Philippe (2016), "Protistes Eucaryotes: Origine, Evolution et Biologie des Microbes Eucaryotes", HAL Archives-ouvertes: 1–462
  4. ↑ Yoo, Yeong Du; Jeong, Hae Jin; Kang, Nam Seon; Song, Jae Yoon; Kim, Kwang Young; Lee, Gitack; Kim, Juhyoung (2010-03-01). "Feeding by the newly described mixotrophic dinoflagellate Paragymnodinium shiwhaense: feeding mechanism, prey species, and effect of prey concentration". The Journal of Eukaryotic Microbiology. 57 (2): 145–158. doi:10.1111/j.1550-7408.2009.00448.x. ISSN   1550-7408. PMID   20487129. S2CID   6312832.
  5. 1 2 Stoecker, Diane K. (1999-07-01). "Mixotrophy among Dinoflagellates1". Journal of Eukaryotic Microbiology. 46 (4): 397–401. doi:10.1111/j.1550-7408.1999.tb04619.x. ISSN   1550-7408. S2CID   83885629.
  6. 1 2 3 4 5 6 Mitra, A.; et al. (2014). "The role of mixotrophic protists in the biological carbon pump". Biogeosciences. 11 (4): 995–1005. doi: 10.5194/bg-11-995-2014 . hdl: 10453/117781 .
  7. 1 2 3 4 Stoecker, Diane K. (July 1999). "Mixotrophy among dinoflagellates". The Journal of Eukaryotic Microbiology. 46 (4): 397–401. doi:10.1111/j.1550-7408.1999.tb04619.x. S2CID   83885629.
  8. 1 2 3 4 5 Jeong, Hae Jin; Yoo, Yeong Du; Kim, Jae Seong; Seong, Kyeong Ah; Kang, Nam Seon; Kim, Tae Hoon (6 July 2010). "Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs". Ocean Science Journal. 45 (2): 65–91. doi: 10.1007/s12601-010-0007-2 .
  9. 1 2 Jeong, HJ; Yoo, YD; Park, JY; Song, JY; Kim, ST; Lee, SH; Kim, KY; Yih, WH (6 September 2005). "Feeding by phototrophic red-tide dinoflagellates: five species newly revealed and six species previously known to be mixotrophic". Aquatic Microbial Ecology. 40 (2): 133–150. doi: 10.3354/ame040133 . ISSN   0948-3055.
  10. 1 2 Skovgaard, Alf (14 December 2000). "A Phagotrophically Derivable Growth Factor in the Plastidic Dinoflagellate Gyrodinium Resplendens (Dinophyceae)". Journal of Phycology. 36 (6): 1069–1078. doi:10.1046/j.1529-8817.2000.00009.x. S2CID   83903548.
  11. ↑ Smalley, GW; Coats, DW; Stoecker, DK (2003). "Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations". Marine Ecology Progress Series. 262: 137–151. doi: 10.3354/meps262137 .
  12. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 Jeong, Hae Jin; Yoo, Yeong Du; Kim, Jae Seong; Seong, Kyeong Ah; Kang, Nam Seon; Kim, Tae Hoon (2010-07-06). "Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs". Ocean Science Journal. 45 (2): 65–91. doi: 10.1007/s12601-010-0007-2 . ISSN   1738-5261.
  13. ↑ Berge, T; Hansen, PJ; Moestrup, Ø (26 March 2008). "Feeding mechanism, prey specificity and growth in light and dark of the plastidic dinoflagellate Karlodinium armiger". Aquatic Microbial Ecology. 50: 279–288. doi: 10.3354/ame01165 .
  14. 1 2 3 Bockstahler, K. R.; Coats, D. W. (1993). "Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay". Marine Biology. 116 (3): 477–487. doi:10.1007/BF00350065. ISSN   0025-3162. S2CID   84468485.
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  16. ↑ Hansen, Per Juel; Cembella, Allan D.; Moestrup, Øjvind (1992-10-01). "The Marine Dinoflagellate Alexandrium Ostenfeldii: Paralytic Shellfish Toxin Concentration, Composition, and Toxicity to a Tintinnid Ciliate1". Journal of Phycology. 28 (5): 597–603. doi:10.1111/j.0022-3646.1992.00597.x. ISSN   1529-8817. S2CID   84540277.
  17. 1 2 Administration, US Department of Commerce, National Oceanic and Atmospheric. "Harmful Algal Blooms". oceanservice.noaa.gov. Retrieved 2017-03-23.{{cite web}}: CS1 maint: multiple names: authors list (link)
  18. 1 2 Hurley, William; Wolterstorff, Cameron; MacDonald, Ryan; Schultz, Debora (2017-03-23). "Paralytic Shellfish Poisoning: A Case Series". Western Journal of Emergency Medicine. 15 (4): 378–381. doi:10.5811/westjem.2014.4.16279. ISSN   1936-900X. PMC   4100837 . PMID   25035737.

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