Negative impacts of Dinoflagellate algae: economic, ecologic, and human health hazards

ABSTRACT Increasing pollution both atmospheric and oceanic are encouraging algal growth and increasing the frequency and geographic range of high density dinoflagellate blooms. Public health and economic impacts, as well as negative ecological effects of the aquatic environment are increasing the scientific research done on toxic dinoflagellate species. Contaminated bivalves are causing paralytic shellfish poisoning (PSP) and diarrhetic shellfish poisoning in humans (DSP); with the number of cases increasing steadily in the last 40 years. Toxins released by certain species of the phylum dinoflagellate are the cause of this spreading contamination. Algal bloom locations are dictated by water currents and synaptic weather patterns, and their movement makes it difficult to pinpoint the origin of these blooms. Measuring the level of toxins in shellfish is currently the best way to chart the growing density of these blooms, and to prove the masses of algae are of growing concern. In this review the negative impact dinoflagellate algal blooms are having on aquaculture, human health hazards, and reasons for the increasing frequencies/densities of blooms will be covered; additional information on the shortcomings of incomplete scientific data complied on algal blooms and why scientific research is now being sought after will be reviewed.

BACKGROUND Few species of phytoplankton produce toxins, but dinoflagellates have species that release two different types of toxins. Dinoflagellates are forming large aggregations called algal blooms with increasing frequency and density. There are two toxins produced by dinoflagellate species: brevetoxins and neuortoxins. Brevetoxins cause the milder human illness diarrhetic shellfish poisoning (DSP), while neurotoxin producing species cause Paralytic shellfish poisoning (PSP), characteristic of temporary paralysis and respiratory failure. Red tides are massive concentrations of harmful neurotoxin releasing species of dinoflagellates and have been reported to being in every ocean and major sea of the world. One of the major impacts of these toxic aggregations of dinoflagellate species is an economic loss for fishing and aquaculture industries. The loss comes from shellfish and marketable fish species contaminated by the toxins released in high levels by dinoflagellate algal blooms. As mentioned before the most dangerous form of dinoflagellate blooms is the Red tide. These blooms tint the surface of the water red, due to the heavy concentration of the single celled phytoplankton, and can release an aerosolized neurotoxin that cause human illness and paralysis after exposure in the form of inhalation (Pierce, 1986). Algal blooms have negative affects on the water it covers, not only from real easing potent toxins but it changes the environment by blocking sunlight from entering past the surface of the water, blocking sunlight from normally photic-zones in the ocean. The competitive dinoflagellate species also cause anoxia in ocean organisms when they use all oxygen in the water and release CO2 in their process of photosynthesis. Algae is at the bottom of the trophic level, which means many larger organisms are affected by the tiny phytoplankton, especially the microscopic predator of dinoflagellate algae, zooplankton. Zooplankton are the primary food of many large ocean mammals and become contaminated when they enter an area covered by a toxic dinoflagellate bloom. Toxins are accumulated in the bodies of zooplankton and can remain there for several days, bringing illness and death to the thousands of larger organisms who rely on zooplankton as a main source of food. A general trophic routing and impact model is proposed in Fig. 1 below, (Smayda 1992). Aquaculture has recently started to have major concern surround dinoflagellate species taking over bioassay tanks, that house several species of finfish that are being decimated by the presence of one of the thousands of species of dinoflagellates. Finfish, is an important group of fish to coastal fishing industries who experience damage to the gills from the armored bodies of dinoflagellate, and the spines extending down the length of their bodies. Table 1 below is a list of all finish, bivalves, and various oceanic wildlife affected by recent increases in dinoflagellate populations. (Anderson et al. 1993). In the following review I will cover impacts toxic dinoflagellate species are having on oceanic organisms and the subsequent effects to aquaculture and fishing industries, and the reasons for increasing frequencies and densities of toxic blooms.

INCREASING ALGAL BLOOMS Algae population dynamics is based on growth, transportation, predation, mortality, and dispersion. The success of an algal population depends on the gains and losses depicted in a basic equation of population dynamics: dN/dt=(Growth+Immigration)-(Predation+Mortality+Dispersion). If the gains are higher than the losses a bloom will occur (Fraga et al. 2012). Losses are due to predation, natural death, and dispersion of parts of the population. A bloom can be split by a violent storm or strong ocean currents. Population gain is mainly due to replication, most marine dinoflagellate species can replicate asexually and sexually, which allows for rapid population growth. The cause of bivalves becoming contaminated are dense aggregations of single cell or several species of dinoflagellate species, that are feeding off of pollution, namely near densely populated coastal areas. The problem of dense algal blooms has increased considerably over the last three decades (Anderson 1995). Reports of toxic blooms went from virtually zero in the 1960's to every coastal state being threatened by these huge aggregations of algae species. Chemicals, fishery products, and loose coastal regulations on pollution have increased the scientific scrutiny of oceanic pollution due to the overwhelming evidence of reports on economic losses, affected resources, and the number of toxic species have all noticeably increased (Work et al. 1993). All of which have conclusive evidence for adding the the problem of increasing toxic algal blooms (Anderson 1995). Dinoflagellate algae are eutrophic phytoplankton with the marine species being made up mostly of autotrophs, meaning they get their nutrients from both photosynthesis and compounds in their environment. Scientific studies on nutrition supply ratios, due to anthropogenic impacts have recently skyrocketed (Smayada, 1990); with pollution normally being thought of as harmful to animals, certain dinoflagellate species namely the toxic ones thrive in these polluted waters. The pollution is bad for a water ecosystem in the first place but toxic algal species are contaminating organisms at the base of the food chain and the increasing frequency of these blooms coupled with the seemingly unstoppable city runoff into the oceans of the world are getting the attention of the media and scientific community. The eastern coasts of Asia, namely Japan and China were the location of some of the first outbreaks of Red tides, and illnesses related to the toxins released by them. Tolo Harbor in Hong Kong has major population growth and as a result has seen a significant increase in water pollution. A 6-fold increase of watershed between the years 1976-1986 caused an observed red tide increase of 8-fold (Lam and Ho, 1989). Run off from densely populated coastal areas is the hypothesized cause of the bloom increase since nutrient loading from pollution feeds the growth of toxic dinoflagellate species. Because Asian coasts have had population density problems for many decades it has some of the only long term studies on the increase of algal bloom population. A long-term study done on the Inland Sea of Japan 44 red tides were reported off the coast in 1965 with a noticeable increase to over 300 red tides in 1975 (Murakawa, 1987). The cause of red tides off the coast of Tolo Harbor forming as a result of excess nutrients from highly populated coastal regions was the reason for the severe increase on the Inland sea on the coast of Japan. A linear relationship is emerging between increases in coastal population and increases in algal bloom frequency. Run off from agriculture plan nutrients have been found to promote toxic algal growth. A small number of studies have found that waters high in plant nutrients experience increases in algal growth as well as an increase in the potency of the brevetoxins released by certain dinoflagellates. This is based on a hypothesis of nutrient ratios and argues that the competitive species of dinoflagellates have toxic species who outcompete other phytoplankton in plant nutrient rich waters (Smayda, 1990). Different types of pollution select for different species of phytoplankton where the more polluted the environment is the less number of species will be present. An extremely polluted pond found on the side of a busy road will typically only have one specie of algae in it, where the common misconception is that heavy pollution will bring greater numbers of dinoflagellate species because of the increase in nutrients. Environmental selectors make it so whichever specie of algae is most fit in relation to the type of pollution present in the water will be the sole specie living there and is the reason for the extreme proliferation of algae near coastal areas.

IMPACT TO ECONOMIC FISHING INDUSTRIES Overfishing in the world's oceans is increasing the demand for aquaculture as an alternative to produce marketable seafood. Predicted market value in aquaculture is projected to pass the total catch of wild fish and shellfish in the next 10-20 years. Demand for shellfish is increasing and with it are reports of paralytic and diarrhetic shellfish poisoning. Dinoflagellate species not endemic to a region can be introduced by the ballast-tank waters in the sediments of bulk cargo vessels. Ballast-tanks discharge the algae into foreign waters when they empty their tanks at different ports, where most species of dinoflagellates can easily adapt to new environments. Aquaculture tanks need to supply finish and shellfish nutrients in the tanks to mimic a natural ecosystem and supply dinoflagellate with an ideal environment to proliferate, with negative impacts on the organisms the industries market. Ocean water is used for aquaculture tanks and dinoflagellates and other phytoplankton are taken up into the tanks containing the fish and shellfish grown in them. Where dinoflagellates can grow inside of these tanks phosphorous, nitrogen, and carbon are being released from marine fish culture systems where feed wastage, fish excretion, faces production and respiration is released into the ocean causing high organic nutrient loadings in coastal waters (Wu, 1995). Increased nitrogen and phosophorous concentrations in pond waters showed large blooms of dinoflagellate development which caused an economic loss for the tested farming industry from shrimp mortality and growth diminution due to toxicity, anoxia, and mucus production effects (Rodriquez and Osuna, 2003) of dinoflagellate species. Dinoflagellates can reproduce at rapid rate with both sexual and asexual mechanisms of reproduction, so the presence of one of these microscopic organisms can infest an entire aquaculture tank. Fish pens in British Colombia are experiencing algal growth in dense concentrations (5000 cells per liter), killing several species of fish: lingcod, sockeye, coho, chinook, and pink salmon (Rensel, 1991). Removal of dinoflagellates from aquaculture tanks is nearly impossible. The microorganisms are incredibly resilient because of cyst formation, and utilization of various nutrients in the water makes several different environments ideal for a number of species. When environmental conditions are unfavorable dinoflagellate species will enter into a resistant resting stage, in order to survive translplantation. A survey of 343 cargo vessels entering 18 Australian ports showed that 65% of ships carried sediment, all of which contained phytoplankton (Hallegraeff and Bolch 1992). Six-teen of the ships carried cysts of toxic dinoflagellate species, that were successfully germinated in the laboratory to produce toxins. These toxic dinoflagellate species, contaminate shellfish with paralytic shellfish poisoning (PSP), and pose a serious threat to human health and aquaculture industry. Techniques to prevent invasive species and unwanted organisms traveling in the ballast-water under large cargo ships are only partially effective in removing dinoflagellate cysts. The cysts are designed for survival, and have hard outer covering and the ability to survive in wet or dry conditions. The effects of fish wastes on algal growth are demonstrated by a spike in the number of laboratory studies that have taken place in the last twenty years (Wu, 1995). Fisheries are experiencing high death rates of finish, an important group of fish to the aquaculture industry. Finfish are being affected by the resilient cysts of dinoflagellates living in the aquaculture tanks. The delicate gill tissue of finfish are being damaged by the armored bodies of dinoflagellate algae penetrating the tissue of the gills. Dinoflagellate algae is known for it's body amour with barbed studs called setae following the length of the body. These studs are hollow and with dense concentrations of algae the studs can break off and pierce the soft gills of the fish, with the barb keeping it from falling out. Fish related deaths can be caused by capillary hemorrhage, dysfunction of gas exchange at the gills, suffocation from an overproduction of mucus, or secondary infection (Bell, 1961). Human consumption of finish exposed to toxic dinoflagellate species is negligible with no reported instances of sickness, but human consumption of bivalves exposed to dinoflagellate blooms have raised concern for public health. In the last decade a total world estimate of 10 billion dollars in economic loss was estimated based on direct killing of marketable shellfish by dinoflagellate contamination. Pearl oysters were exposed to the dinoflagellate specie Heterocapsa circularisquama in a study conducted by Matsuyama (1996), where all bivalve test subjects died within a couple days after exposure. The dead pearl oysters had noticeable shrinkage to the mantle part of the body, and internal discoloration of the gut. Similar results were found in a field survey done in Hiroshima Bay. After an outbreak of dinoflagellate algae bivalve species were reported to have a reduced filtration rate and cell density below 1% (Li, Wu, and Hsieh 2002). In lab experiments using pearl oysters as the test subject, the bivalves experienced unusual contraption of the mantle, and gills, and sustained valve closure, paralysis and death within 24 h, when dinoflagellate algae was added to the enviornment of the pearl oysters with a cell density of 10^7 cells L^-1 (Matsuyama 1998). Dinoflagellate genera such as Gyrodinium and Aureococcus form what is referred to as brown tides that are non-toxic tides with a brown coloration reported to cause considerable failure in mussel and scallop farming (Shumway 1990). Although non-toxic brown tide forming dinoflagellate species were found to do considerable damage to various bivalve species. The brown tide forming genera are not species specific in harming marine animals, so the list of organisms they affect is open ended and growing. Different species of dinoflagellates cause different problems, Heterocapsa circularisquama, causes kill offs of shellfish, which is an economic hit for fishermen. While dinoflagellate genera Alexandrium, Gymnodinium, and Dinophysis, cause shellfish poisoning which cause human illness, as mentioned before. Genera such as Heterocaspa kill large amounts of bivalves in aquaculture containing these specific types of dinoflagellates as well as in the wild. HAZARDS TO HUMAN HEALTH Paralytic shellfish poisoning is caused by aerosolized neurotoxins with increasing numbers of outbreaks steadily growing each year. Neurotoxin producing dinoflagelltae blooms of Alexandrium tamarense and Gonyaulax cantenella were reported to be exclusively found in temperate waters of Europe, North American and Japan (Dale and Yentsch, 1978). In the early 1990's paralytic shellfish poisoning outbreaks were documented in every major ocean and most major sea of the world. The most afflicted areas are coastal regions, with high amounts of ocean traffic and dense populations, both contributing to water pollution that is feeding the autotrophic phytoplankton. Japan was one of the first countries to report an outbreak of paralytic shellfish poisoning, and between 1978 and 1982 the number of areas affected in Japan increased from 2-10 (Anraku 1984). In humans two distinct sicknesses, depending on the type of exposure, are associated with brevetoxins released by dinoflagellate algae (Kirkpatrick, Fleming and Squicciarini et. al. 2004). Ingestion of brevetoxin contaminated ocean animals causes gastroenteritis and is classified as diarrhetic shellfish poisoning (DSP). DSP pales in comparison to the neurologic symptoms and respiratory problems experienced but those exposed to aerosolized neurotoxins in Paralytic shellfish poisoning (PSP). As the name implies PSP causes temporary paralysis and respiratory problems in humans, lasting up to 24 h. Guatemala saw an outbreak of PSP where 18 people were affected, with neurological symptoms and 27 deaths (Rodrigue et al. 1990). Inhilation of aerosolized brevetoxins is possible from sea spray containing the red tinted dinoflagellates that make up red Tides, or simply by boating over an area of water covered with a bloom if the toxic species (Fleming and Baden, 1988). Ocean organisms that ingest phytoplankton or bivalve contaminated with neurotoxins or brevetoxins have been found to die due to internal complications, which is a double hit for fishing industries who not only lose contaminated bivalves and fish but also lose sea animals that feed on the contaminated species. A red tide located off the southwest coast of Florida provided much needed data compilations of the health hazards related with the genus Gymnodinium, humans exposed to the aerosol released by the dinoflagellates experienced respiratory irritation, contact irritation, and shellfish in the covered area were found to contain neurotoxic poisoning (Hemmert, 1975). A study done in 1987 by White, compiled a dataset of PSP toxin concentrations with the ratio of JLg saxitoxin equivaient/IOO g shellfish meat, in Bay of Fundy clams, where monitoring started in 1944. Figure 2 shows the increased frequency of dinoflagellate blooms at this site starting in the 1970s and going through the early 1980s. No major outbreaks have been recorded since, but this goes back to the original problem with data collection in that the blooms have unpredictable movements, and could be easily missed if a site isn't check on every day, which is not realistic considering blooms are found in every marine habitat on Earth.

ECOLOGICAL IMPACTS The harmful effects of red tides and high density algal blooms are die-offs from anoxia or hypoxia and mechanical or physical damage to every level of the trophic level (Pitcher and Calder, 2000) Bivalve shellfish and zooplankton are the two organisms most heavily affected by brevetoxin contamination. Both are filter feeding organisms, and high concentrations of toxic dinoflagellate's mean large amounts of brevetoxins are being released into the water. Bivalves and zooplankton feed on phytoplankton and other microscopic organisms and chemicals in the water and obtain their energy by filtering the water in the environment through their bodies. When brevetoxins are present in the environment both bivalves and zooplankton have shown signs of accumulation of these toxins, and upon ingestion cause the human illnesses previously mentioned and death in oceanic birds and animals. Laboratory studies on Prorocentrum minium, a toxic dinoflagellate known to cause shellfish toxicity demonstrate isolated toxins of this specie killed mice on injection (Wikfors, 2005). The toxins causing diarrhetic shellfish poisoning have no apparent effect on the bivalves that accumulate toxins in the epipoidal fringe, or main body of the shellfish. The epipodal fringe is the part of shellfish marketed by fishing industries. Toxins in shellfish are undetectable, with contaminated shellfish being reported only after human ingestion and contraction of DSP or PSP. The gastrointestinal irritations caused by the brevetoxins accumulated in shellfish have the same symptoms as food poisoning. Laboratory studies have shown the effects dinoflagellate species have on shellfish larvae are systematic immune responses in oyster and scallops (Wikfors, 2005). Traditionally scientific monitoring has been focused on filter-feeding organisms, but efforts are now being turned to higher0rder consumers such as carnivorous, gastropods, and crustaceans (Shumway, 2008). Expert Consultation on Biotoxins aimed at assessing the number of biotoxins present in bivalve mollusks has developed a risk assessment test to categorize the biotoxins produced by dinoflagellate algae. Eight different groups of toxins have been divided based on the chemical structure of the toxin (Toyofuku, 2006). Safety factors are applied through animal testing, but the database for brevetoxins was insufficient to establish provisional resistance drugs for this group of toxins. The increase of red tide and other algal blooms can be seen at international conferences used to report outbreaks of PSP and DSP as well as the location and number of algal aggregations off the coasts of participating countries. Harmful algal blooms increasing globally, sparked the International Symposium on Red Tides, a specialized conference where countries reported PSP and DSP yearly (Anderson 1989). In 1972 New England expressed concern of spreading aggregations of red tinted algae. In 1978 Paralytic shellfish poisoning outbreaks were reported being spread through Spanish mussels. From 1972 to 1985 the symposium for Red tides grew from 3 participating countries to 27. At the 1987 Symposium on Red Tides, more new outbreaks have been described than ever before in locations including Rhode Island, New York, Tasmania, Taiwan, Guatemala, Korea, Hong Kong, and Venezuela.
RESEARCH
Most recent studies conclude planktonic species of dinoflagellates are having the greatest ecological impact, with emphasis on the genera Ostreopis and Gambierdiscus (Fraga et al. 2012) on ocean ecosystems. Many unanswered questions about the fundamental ecology of dinoflagellate, toxic species in particular because of the size of this class of algae, critique of accuracy noted inadequacies ranging from inconsistency to sensationalism and misinformation. The use of improved web-based information sources is the best method to improve communication between scientist, journalists and the public. The worlds scientific literature provides little discussion of brevetoxins and related public health problems, but growing reports of outbreaks are increasing the appeal for laboratory studies. Literature on toxic algal blooms and red tides have increased with the increasing global frequency, magnitude, and geographic extent of these events in the last two decades. The increase of research is undoubtedly a result of the increased awareness and analytical capabilities to study microorganisms of the scientific community, and the movement of these blooms being made possible by major water currents and storm cells (Anderson, 1989). Evidence of the distance blooms are transported is not conclusive, with controversial hypothesis and unknown scales of spatial miles/kilometers from the past. New scientific studies have no data to compare against, with regard to the increase in size and density of algal blooms. The biggest pitfall in studies on algal blooms such as red and brown tides are that there is not enough past data to compare boom outbreaks to. Part of the reason or this is that the technology to effectively study microscopic phytoplankton. With toxic species of dinoflagellates one's that release toxic aerosols have immediate affects after exposure and original studies on red tides species were incomplete due to those involved exhibiting the symptoms of respiratory problems and paralysis. The best studies are from Asian coastal regions, providing data dating back to the 1970's. Another problem in compiling a complete data set is that many outbreaks are in temperate waters near the equator, surrounding poor countries that do not have the capabilities of United State and European laboratories. The best way to create a complete data base involving toxic dinoflagellate species and blooms is to increase the number of countries involved in the International Symposium for Red Tides. Slowing the increased frequency of algal blooms will be accomplished through coastal pollution regulations and population caps.
CONCLUSION
Dinoflagellate algae is the second largest group of eutrophic phytoplankton, that is gaining international appeal for laboratory studies based on the human illnesses and negative ecological impacts dense aggregations of dinoflagellates. Aquaculture and fishing industries are experiencing economic losses, due to the toxins released by certain dinoflagellate species. Oceanic pollution supplies nutrients to dinoflagellate algae, especially in coastal areas are seeking regulations to decrease the nutrient surplus supplied by the pollution that encourages algal growth. Through international communication and oceanic pollution regulations coupled with increased laboratory studies and improvements in detecting toxins in marketed ocean animals will all help to decrease the negative impacts humans and the worlds oceans are experiencing from dinoflagellate algae.

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