Harmful Algal Blooms

Phytoplankton and Biotoxin Monitoring Programs

Connecticut has a thriving shellfish industry and has reliably produced safe clams and oysters for locals and visitors to enjoy. Although Connecticut has not experienced a harmful algal bloom (HAB)- related closure since 2003, the Department of Agriculture Bureau of Aquaculture (DA/BA) has consistently maintained phytoplankton and toxin monitoring programs as an early warning system, and collaborates with partner agencies to respond to potential HAB events and fish kills. DA/BA initiated the biotoxin monitoring program in 1985 and phytoplankton monitoring program in 1997.

Microalgae, or phytoplankton, are the base of the marine food web and support filter- feeding shellfish, are critical for marine nutrient cycling, and produce 50% of the oxygen on Earth. Therefore, phytoplankton are important locally and globally, despite their microscopic size. A small percentage of microalgae are classified as HAB species. Although HAB species are only visible under a microscope, they can form blooms that are evident to the naked eye as discolored water. HABs are deemed harmful because they are associated with toxin production and have detrimental effects on human health and the environment. Marine and/or freshwater HABs impact every single state in the United States.

HAB species and their associated toxins can be filtered out of the water column by bivalve shellfish, like oysters and clams. Some toxins can be lethal when concentrated in shellfish tissues. Since state programs, like DA/BA, routinely monitor for the presence of HABs and their associated toxins, consumers affected by shellfish poisonings have typically illegally harvested shellfish from closed recreational beds. When toxin concentrations in shellfish near or exceed established levels, DA/BA immediately closes impacted shellfish growing areas.

Additionally, DA/BA monitors HAB species that do not produce toxins and therefore do not pose a human health risk, but are detrimental to the shellfish or finfish industries.

Regulation of HAB Species

In accordance with the FDA, DA/BA is primarily concerned with the five regulated shellfish poisoning syndromes, Paralytic Shellfish Poisoning (PSP), Amnesic Shellfish Poisoning (ASP), Diarrhetic Shellfish Poisoning (DSP), Neurotoxic Shellfish Poisoning (NSP), and Azaspiracid Shellfish Poisoning (AZP). The National Shellfish Sanitation Program Model Ordinance (NSSP-MO) outlines mandatory toxin closure levels and guidelines for how all FDA- approved programs should monitor HABs and biotoxins. DA/BA maintains a Biotoxin Contingency and Management Plan, which outlines how staff members monitor for the presence of HAB species and their associated biotoxins, how DA/BA will respond and close shellfish growing areas if the toxins are detected, and how DA/BA will reopen closed areas once toxin levels return to undetectable levels.

NSP is largely isolated to the Gulf of Mexico and the southern east coast; however, range expansions of the causative organism Karenia have been documented. Karenia mikimotoi was recently found in the Gulf of Maine (Leach 2018), and 1) can lead to low oxygen levels (hypoxia) following a bloom and 2) has been shown to produce cytolytic and hemolytic compounds that can cause fish kills. Karenia brevis and Karenia papilionacea, which produce brevitoxins and can cause NSP, have been identified in Delaware (Bott 2014; Fowler et al. 2015). AZP, caused by Azadinium and Amphidoma, is an emerging issue largely isolated to Europe; no AZP cases have been reported from U.S. shellfish. Therefore, NSP and AZP are not currently expected to occur in Connecticut.

Paralytic Shellfish Poisoning

When a phytoplankton bloom turns the water red or brown, the event is commonly referred to as a "red tide." Toxic and non-toxic species have caused red tides around the world, although red tides are typically synonymous with toxic species. Additionally, multiple toxic species are associated with red tide in the United States. The confusion surrounding the term "red tide" can cause concerns about water quality and local seafood, miscommunications about public health issues, and economic losses due to reductions in recreational activities and tourism.

New England red tide is caused by the dinoflagellate Alexandrium. Alexandrium produces a potent neurotoxin called saxitoxin. Paralytic shellfish poisoning (PSP) is the syndrome associated with the consumption of shellfish contaminated with saxitoxin. PSP symptoms may include, tingling, numbness, burning in the extremities or mouth, lack of coordination, drowsiness, nausea/vomiting, diarrhea, fever, and rash. In extreme cases, PSP symptoms can include respiratory arrest and death if not provided supportive care at a hospital. New England red tide is naturally occurring and has been documented for hundreds of years. Native Americans even developed a method for identifying when shellfish were not safe to consume before the cause of shellfish poisonings was known.

New England red tide has become predictable, with extensive monitoring occurring from April to October. While northern New England states such as Maine began to have annual PSP closures in the 1970's, southern New England states such as Connecticut and Rhode Island, as well as New York historically had sporadic, smaller- scale closures. However, HAB patterns in southern New England are changing, and New York now annually experiences at least five types of HABs (one of which is red tide), a characteristic potentially unmatched in the United States (Hattenrath-Lehmann and Gobler 2016). Despite Alexandrium's documented presence in New York since the 1980's, extensive, near- annual closures did not occur until 2006 (Hattenrath et al. 2010). Although Alexandrium has been documented in Connecticut since the 1980's (Anderson et al. 1982; Anderson 1986; WHOI 1999), shellfish beds have only experienced closures in 1985, 1992, and 2003. Similar to how plants produce hardy seeds that can germinate the following spring, Alexandrium produce hardy cysts that lay dormant in the sea sediment. Once conditions become ideal, typically in the spring, Alexandrium emerge from their cysts and can potentially form toxic blooms as planktonic (free-swimming) cells. Additionally, Alexandrium cells have been identified at low concentrations in areas that have not previously been closed due to PSP throughout Long Island Sound (DABA, unpublished data; Gobler and Hattenrath-Lehmann 2011). There have been no PSP- related illnesses in Connecticut.

Amnesic Shellfish Poisoning

The diatom Pseudo-nitzschia produces a potent neurotoxin, domoic acid. Amnesic shellfish poisoning (ASP) is the syndrome associated with the consumption of shellfish contaminated with domoic acid. ASP symptoms may include dizziness, headache, disorientation, and short-term memory loss. There are also gastrointestinal ASP symptoms such as nausea, vomiting, abdominal cramps, and diarrhea. In extreme cases, ASP symptoms can include seizures, respiratory difficulty, coma, long-term neurological damage (including memory defects and weakening or death of muscle in the extremities), and death. In addition to shellfish, planktivorous (low-level, plankton feeding) fish and crabs are potential vectors for ASP in humans (see Di Liberto 2015 for more information). Pseudo-nitzschia have caused substantial marine mammal and seabird illness and mortality events, particularly on the west coast of the U.S. For example, de la Riva et al. (2009) showed that 2,239 marine mammals, including California sea lions and common dolphins, stranded in 2002 making this an "unusual mortality event," in association with Pseudo-nitzschia. Additionally, Pseudo-nitzschia have caused long closures of shellfish beds due to persistently high and unsafe toxin levels, such as season-long closures of razor clam beds in Washington State in 1998- 1999 and 2002- 2003 (estimated $24.4 million annual value) (Dyson and Huppert 2010). Recent research is also showing that consuming low levels of domoic acid via shellfish or another vector over a long period of time may cause memory problems, prompting Washington State to issue an interim advisory for limiting razor clam consumption on the west coast (WA DOH 2016).

The first ASP closure in New England occurred in 2016. Part of the Gulf of Maine was mandatorily closed in September 2016 and five tons of mussels and clams were recalled. The Pseudo-nitzschia australis bloom and its associated toxicity had a rapid onset, with shellfish accumulating 3-4 times the FDA domoic acid closure limit within just 22 days. Pseudo-nitzschia australis also reached Massachusetts and Rhode Island, which instituted precautionary closures. Then in March 2017, a Pseudo-nitzschia australis bloom was detected in Rhode Island and prompted a mandatory closure due to the detection of domoic acid over the FDA closure limit. Maine saw a resurgence of Pseudo-nitzschia australis in September 2017 and again had to recall shellfish product. After the rapid onset of shellfish toxicity and two major recall events (2016, 2017), Maine started to institute precautionary closures prior to domoic acid levels reaching the FDA closure limit. Presentations with information about these and related Pseudo-nitzschia events are available online: (Hubbard, 2018 & Kanwit, 2018).

Pseudo-nitzschia, including some toxic species, are native to Long Island Sound. However, no human or animal ASP events have been reported in Long Island Sound.

Diarrhetic Shellfish Poisoning

The dinoflagellates Dinophysis and Prorocentrum produce the toxin okadaic acid and its derivatives, the dinophysistoxins. Diarrhetic Shellfish Poisoning (DSP) is the syndrome associated with the consumption of shellfish contaminated with okadaic acid and its derivatives. DSP symptoms may include nausea, vomiting, abdominal pain, and incapacitating diarrhea. Individuals with DSP typically recover within three days, but consumers with predisposed conditions may require hospitalization to treat fluid and electrolyte imbalance. While DSP is one of the least severe shellfish syndromes, it can be underreported due to misdiagnosis as viral or bacterial contamination. Additionally, okadaic acid is a carcinogen (Fujiki and Suganuma 1999; Suganuma et al. 1988, 1989) and could potentially cause cancer from long term exposure.

The first local bloom of Dinophysis acuminata was discovered in Northport Harbor, Long Island, NY in 2008. In Northport Harbor in 2011, D. acuminata reached over one million cells/L, making this the largest recorded bloom in North America, and some shellfish tested at over seven times the FDA closure limit (Hattenrath-Lehmann et al. 2013).

Over 10 different Dinophysis species have been identified in Long Island Sound and its surrounding areas (Fredudenthal and Jijina 1988). Dinophysis acuminata and Dinophysis norvegica are the most common Dinophysis species in Connecticut, and both are known to produce toxins. A potential new toxin was recently discovered from D. norvegica in the Gulf of Maine; however its toxicity still must be determined. More information can be found in the following presentation: Deeds 2019.

While DSP events are typically associated with Dinophysis, some Prorocentrum species also produce okadaic acid and its derivatives. Toxic Prorocentrum tend to be benthic and do not have spines. Conversely, non-toxic Prorocentrum tend to be planktonic and have spines. Currently, Prorocentrum lima (toxic), Prorocentrum minimum (toxic to shellfish), Prorocentrum scutellum (non-toxic), Prorocentrum micans (non-toxic), and Prorocentrum triestinum (non-toxic) have been documented in Connecticut.

P. lima is distributed throughout the northeast and produces toxin (Maranda et al. 2007 a&b). Planktonic concentrations of P. lima do not necessarily reflect concentrations in shellfish because it is a benthic species and typically is not seen in the water column (Morton et al. 2009), making it a difficult species to monitor. P. lima can cause shellfish toxicity following storms that disturb the sediment or when present in association with macroalgae that directly or indirectly foul shellfish (Morton et al. 2009). P. minimum was shown to cause mortality in scallops and growth inhibition in clams (Wikfors and Smolowitz 1993). P. minimum also alters the immune system of juvenile oysters and scallops (Hegaret and Wikfors 2005), blue mussels (Galimany et al. 2008), and northern quahogs (Hegaret et al. 2010). Additionally, some P. minimum strains may produce toxins (Rodriguez et al. 2017; Vlamis et al. 2015); however, additional research is necessary. While P. scutellum, P. micans, and P. triestinum are non-toxic species, they can cause hypoxia after blooming.

No DSP illnesses have been reported in Connecticut.

Environmentally Disruptive HAB Species

A Margalefidinium polykrikoides (formerly Cochlodinium polykrikoides) bloom was first reported in the area in the 1980's when cell concentrations exceeded three million cells/L in Rhode Island (Tomas and Smayda 2008). M. polykrikoides was first reported in Long Island Sound in 2002 (Gobler et al. 2008). Dense blooms started in 2004 and now typically occur annually around Long Island, NY in the late summer/ early fall in Long Island Sound (Gobler et al. 2008). A massive soft shell clam mortality event in Flanders Bay was associated with M. polykrikoides cells, which were present in the hemorrhaged digestive tracts of the clams (Gobler et al. 2008). It has been proposed that M. polykrikoides cells may produce toxins that cause fish and shellfish mortalities and larval and metamorphosing shellfish as well as larval and juvenile fish are most susceptible to these putative toxins (Tang and Gobler 2009). Exposure to M. polykrikoides has resulted in increased mortality and decreased growth, as well as inflammatory responses and hemorrhage of the gills and gut, in bay scallops (Gobler et al. 2008). Additionally, Eastern oysters exposed to M. polykrikoides experienced increased mortality and cell death in the gills and digestive gland (Gobler et al. 2008). Since 2008, M. polykrikoides has sporadically been reported in Connecticut waters. While mortality events have not concretely been associated with M. polykrikoides to date, it is likely that it is having consistent negative impacts on shellfish survival and recruitment.

Akashiwo sanguinea is also present in Long Island Sound and has been attributed to invertebrate, fish, and seabird mortality events around the world. A. sanguinea was shown to produce a surfactant-like material that impacted water-repelling abilities of feathers, resulting in the stranding of 550 and the death of over 200 seabirds from 14 different species in Monterey Bay in 2007 (Jessup et al. 2009). Two mortality events involving at least 10,500 seabirds in September and October 2009 along the Washington State coast were attributed to A. sanguinea, making this the largest definitive seabird mortality event ever attributed to a single HAB species (Jones et al. 2017). A. sanguinea was shown to be toxic to invertebrates, shellfish, and finfish (Xu et al. 2017). A. sanguinea was also shown to consistently cause significant mortality in abalone larvae during a laboratory experiment (Botes et al. 2003). Abalone, valuable warm-water molluscs, are harvested from the wild and grown in mariculture operations for consumption and their unique mother-of-pearl shells.

Conclusions

Neighboring states New York and Rhode Island are managing emerging toxic HAB events that have not yet caused closures in Connecticut. The emergence of HABs strains local industries such as the shellfish industry and requires additional monitoring efforts by regulatory agencies such as Connecticut DA/BA. There is a general consensus among scientists that the intensity and frequency of HABs are increasing around the world. With the increasing threat of HABs globally, the reoccurrence of many harmful species along the New York border of Long Island Sound and neighboring Rhode Island waters, along with much still to be learned about what causes and controls HABs, DA/BA is continually prepared for a potential future bloom and any associated consequences for the shellfish growing areas, harvesters, and consumers.

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