Toxins and Toxins Secreted by Algal Bloom Habitats: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Jessie Wu and Version 1 by Dominik Metelski.

Fish die-offs are important indicators of aquatic environmental problems, and although some fish species are very sensitive to adverse changes in environmental conditions (there are many fish species that have a relatively low tolerance to changes in the environment), it is important to remember that such changes usually affect entire aquatic ecosystems, and thus other animals and plants, as well as everything related to the bottom life of the aquatic environment. Localized sudden and mass fish kills or even whole fish populations and deterioration (mortality) in aquatic life in different types of water bodies, namely freshwater, marine, and estuarine, have been observed quite frequently and excessively in recent years. Although the causes of their occurrence may be natural, anthropogenic changes and pollution (including toxins) in aquatic and terrestrial systems are major contributors to the increasing frequency and magnitude of fish kills worldwide.

  • harmful algal blooms
  • ecological catastrophe
  • prymnesins
  • river ecosystem
  • aquatic toxicity
  • water pollution
  • environmental monitoring
  • eutrophication
  • microalgal ecology
  • fish kill

1. Toxins

Toxins can pose a lethal threat to aquatic fish for several reasons They can, for example, (1) damage gills and other organs, making it difficult for fish to breathe and survive; (2) disrupt the nervous system, leading to disorientation, paralysis, and death [23][1]; (3) damage the liver, kidneys, and other organs, leading to organ failure and death [24][2]; (4) disrupt the hormonal system, leading to reproductive failure [25,26,27][3][4][5]; (5) disrupt the immune system and make fish more susceptible to disease [28,29][6][7]; (6) impair fish growth and development, leading to abnormal growth or even death [30][8]; and (7) accumulate in fish tissues and can be passed through the food chain, making fish unsafe for human consumption [31][9]. It is important to know that toxic substances can come from many sources, including industrial pollution, agricultural runoff [32[10][11],33], and even naturally occurring toxins produced by certain species of algae or bacteria [34,35][12][13]. It is important to monitor water bodies and take steps to reduce or eliminate sources of toxins to protect fish populations and the ecosystem as a whole. The following are some examples of specific toxins that can contribute to ecological disasters and the mass mortality of fish: (1) Ammonia—a toxic compound that can enter water bodies through agricultural runoff [36][14], industrial effluents, and other forms of pollution. High levels of ammonia can impair the respiratory capacity of fish and lead to mass fish kills [37,38][15][16]. (2) Heavy metals such as lead, mercury [39[17][18],40], and cadmium can be toxic to fish, and high concentrations of these compounds can cause mass fish kills [41][19]. Heavy metals can enter waterways through industrial wastewater, agricultural runoff, and other forms of pollution. (3) Polychlorinated biphenyls (PCBs)—a group of chemicals that were widely used in industry and are now banned in most countries. PCBs can remain in the environment for decades and can be toxic to fish [42][20], leading to massive fish die-offs [43,44,45][21][22][23]. (4) Cyanide, which can also be toxic to fish and leads to massive fish kills [46][24]. Cyanide can enter waterways through industrial wastewater, agricultural runoff, and other forms of pollution. (5) Oil spills, which can cause massive fish kills by smothering fish and disrupting oxygen levels in the water [47,48][25][26]. (6) Pesticides—toxic to fish and cause massive fish kills [49][27]. Pesticides can enter waterways through agricultural runoff and other forms of pollution [50][28]. (7) Algal blooms—some harmful algal blooms can produce toxins that can be lethal to fish and other aquatic life and cause massive fish kills [14,51,52][29][30][31]. It is important to note that the toxins that cause mass fish kills can vary by location and pollution source. It is important to investigate and understand the cause of fish kills to prevent future incidents and protect the aquatic ecosystem.
There are numerous examples in the literature of mass deaths of fish caused by the presence of toxins in the aquatic environment. Most often, such cases occur in connection with the discharge of substances into water bodies that are directly toxic or cause a change in the pH of the water or its temperature. Harmful substances that enter water bodies (aquatic environments) as a result of anthropogenic activities may themselves be toxic (cause toxicity) or cause a change in the properties of the water, such as its pH or temperature, which may subsequently lead to mass fish kills. Larson et al. [53][32] described fish kills in the United States caused by pesticides, particularly endrin. Researchers refer to numerous cases of fish kills caused by the mixing zone effect [54][33], i.e., harmful interactions between acid, calcium, and labile aluminum at certain concentrations [55][34] or chemical interactions with complex polymeric aluminum salts [56][35]. Rosseland et al. [54][33] described in detail the phenomenon of mixing zones and chemical imbalances caused by transformation processes. Such mixing zones occur near acidic tributaries and stream limestones. For example, it was the effect of the mixing zone that was responsible for the near extinction of the perch population in the L. Iso Valkjaervi watershed in the early 1990s. Supersaturated aluminum solutions with their persistent active precipitates proved to be particularly toxic to fish. This phenomenon was confirmed with experiments in a mixing zone in the limed Audna River in Norway. Rosseland et al. [54][33] studied the stress to which Atlantic salmon and sea trout were subjected by mixing acidic and calcareous water downstream of the crossing. In the acidic tributary, the LT50 (a term used in toxicological studies that refers to the median lethal time, i.e., the time that elapses before 50% of a test population dies after exposure to a toxic substance or stress condition; it is commonly used to quantify the amount of a stressor necessary to kill an organism) was 22–40 h (depending on the fish species), while in the mixing zone (different pH parameters, Ca in mg/L and Ali), LT50 was 7 h for both species. Thus, due to the conversion of Al into high-molecular-weight precipitation species, failure of osmoregulation and lethal changes in fish gills occurred in the mixing zone. The results indicate greater toxicity of the mixing zones on the health status of fish than in acidic and Al-rich water.
It is important to emphasize that cases of toxic conditions are more likely in poorly buffered water. Accidental discharges of various chemicals, such as acidic process water, are not uncommon. One example is the 1997 discharge of acidic process water into Skinned Sapling Creek that accidentally occurred at a phosphate plant in Mulberry, Florida. At that time, tens of millions of gallons of acidic water were discharged into Skinned Sapling Creek, significantly lowering the pH of the water (from 8 to 4) [57][36] and contributing to the mass mortality of more than one million fish [57,58][36][37]. The discharge of acidic process water from a phosphate plant could be caused by a failure in the plant’s safety systems, such as a leak in the retention pond or a malfunction in the treatment process. This type of discharge can have significant environmental impacts, such as the death of fish and other aquatic life, and can also have economic impacts on local communities that depend on fishing and tourism. Acidic industrial process water can contain a variety of toxins, including heavy metals and other pollutants, depending on the specific industrial process. These toxins can be harmful to both human health and the environment if not properly managed. In addition, acidic industrial process water can also cause environmental damage if discharged into natural waters. It is important to know that acidic industrial process water should be treated before it is discharged into the environment. Treatment options include neutralization to raise pH, precipitation, and flocculation to remove heavy metals and other pollutants, and biological treatment to remove organic pollutants. The specific treatment options depend on the type and concentration of contaminants present in the process water [59][38]. It is also important to know that regulations for the treatment and discharge of industrial process water vary by region and industry. Therefore, it is important to contact the appropriate authorities to ensure compliance with all applicable regulations. Other cases include an accidental spill of bourbon whiskey into the Kentucky River in 2000 [60][39]. The incident occurred when Wild Turkey’s whiskey warehouse caught fire. At that time, several thousand barrels of burning whiskey spilled into the surrounding area, with about 20% of the whiskey entering the Kentucky River, resulting in a reduction in oxygen levels in the water and a mass mortality of about 228,000 fish in a 66-mile stretch of the river. In 1999, a fish kill in the White River in Indiana was caused by a chemical spill. The cause of the fish kill was initially unknown, but ammonia contamination was suspected [61][40]. The investigation traced back to Guide Corp, a manufacturer of automotive lamps that had discharged toxic waste into the river [62][41]. In 2011, the Temple-Inland paper mill in Bogalusa, Louisiana, discharged chemicals into the Pearl River, causing a massive fish kill [63][42]. In 1995, a 120,000-square-foot lagoon at Oceanview Farms in North Carolina burst and discharged twenty-five million gallons of fecal matter and sewage into the New River [64][43]. This killed at least ten million fish and polluted 350,000 acres of coastal shellfish habitat. A fish kill in Michigan’s Tittabawassee River in 2020 was caused by pollution from a toxic waste dump (as a result of the Edenville Dam collapse) [65][44]. In 2023, hazardous materials were released into the Tittabawassee River and transported downstream to the Saginaw River and Bay [66][45]. In the past, there have been even more serious ecological disasters involving fish kills associated with the Tittabawassee River. In 1986, up to 30 million gallons of diluted chemicals entered the Tittabawassee River, resulting in fish contamination (tainting) [67][46]. The incident had significant environmental impacts, including the death of hundreds of thousands of fish. According to another source, an industrial spill in the mid-1960s killed an estimated 14,000 fish in the Tittabawassee River near Midland [68][47]. In 2017, PFAS contamination of drinking water and fish was discovered in the Huron River in southeast Michigan [69][48]. Fish kills can also be caused by toxins produced by harmful algae. There are many species of harmful algae, and one of them is P. parvum, which is cited as the main cause of the 2022 disaster in the Odra River, which is analyzed in more detail in this researticlech. Therefore, this particular species of algae will be discussed in more detail in Section 2.2 and subsequent sections.

2. Algae Blooms and Harmful Toxins Secreted by Habitats of Algal Blooms

There are several types of harmful algal blooms that can release toxins that can be lethal to fish. The most common types of harmful algal blooms include red tide (Karenia brevis) [70,71][49][50], cyanobacterial blooms [72[51][52],73], brown tide (Aureococcus anophagefferens) [74][53], diatom blooms [75][54], and P. parvum (also known as golden alga) [76,77,78][55][56][57]. These blooms can produce different types of toxins that can cause various symptoms in humans and animals. It is widely recognized that there are more toxic algal species today than in the past, which has led to higher economic losses and impacts on fisheries resources [79][58]. Algal blooms occur when nutrient concentrations in the water are elevated, due to the discharge of wastes and fertilizers (or other chemicals) into the water. Heisler et al. [80][59] note that degradation in water quality due to increasing nutrient pollution promotes the development and persistence of many harmful algal blooms. The Centers for Disease Control and Prevention (CDC) explain that harmful algal blooms usually form in warm waters with high levels of nutrients such as nitrogen and phosphorus [81][60]. The US Environmental Protection Agency (EPA) and National Oceanic and Atmospheric Administration (NOAA) also state that harmful algal blooms require nutrients (nitrogen and phosphorus) to form [82,83][61][62]. It is worth noting that not all species of algae should be associated with the secretion of toxins that are harmful to fish (only some). Algae are dangerous to fish because—when they die and decompose—they lead to a reduction in the oxygen content of the water (deprive it of oxygen), which under the right conditions (high temperature, too low or too high pH) can be the cause of mass fish death. Very often, mass mortality of fish is attributed to a combination of several of the above causes (higher temperatures, low water levels, and algal blooms). This was the case, for example, in Lake Peipsi in Estonia in the summer of 2002, where massive fish kills were caused by the synergistic effect of high temperature, low water levels, and a blue–green algal bloom [84][63].
The first mention of algal blooms associated with P. parvum (indicated as the causative agent of the 2022 Odra disaster) was published by Liebert and Deerns in 1920 [78][57]. However, it should be noted that a detailed description of P. parvum based on specimens from a brackish pond at Bembridge on the Isle of Wight was published by Carter in 1937 [85][64]. Moreover, the prymnesins were first isolated only in the late 20th century (1995 to be precise) [86][65]. Relevant comments on the systematic classification (arrangement) of haptophytes, taking into account their taxonomy at the species and morphological levels, can be found in the work of Larsen [87][66] and Edvardsen et al. [88][67]. Furthermore, P. parvum (N. Carter) was well-documented and described in the 1960s by Manton and Leedale [89][68] and Manton [90][69]. P. parvum is a species of haptophyte, a group of microalgae characterized by the possession of haptonemes, slender whip-like appendages that aid in motility. The cells of P. parvum are typically 3.5–11 µm wide and 6–18.5 µm long [91,92][70][71] (see Figure 1).
Toxins 15 00403 g001 550
Figure 1.
P. parvum (N. Carter 1937) [85].
(N. Carter 1937) [64].
P. parvum is a species of golden alga that has flagella and chloroplasts for photosynthesis [93][72]. It has a complex life cycle that includes both sexual and vegetative phases. This microalgae species is known for its coccolith production and its ability to produce a toxic compound that is harmful to other aquatic animals. It can form blooms in freshwater and marine systems and negatively impact the ecosystem and water quality. According to Roelke and Manning [76][55], the life cycle of P. parvum has three stages: two haploid stages, one diploid stage, and a survival stage called a cyst.
There is extensive literature describing cases of P. parvum. This researticle ch focuses on the analysis of P. parvum and the harmful toxins prymnesins secreted by these algae, which are considered to be the direct cause of the environmental disaster in the Odra River in 2022. Therefore, selected cases that occurred in different countries are briefly characterized in Table 1.
Table 1.
P. parvum
cases in different countries.
Case Study Description Country/Authors
In 2009, a devastating P. parvum bloom occurred at Barramundi Farm in Australia, resulting in the loss of all fish in the ponds. In response, a number of measures were taken to prevent similar incidents in the future [94]. To this end, an experimental manipulation of nutrients and pH was conducted in one of the ponds. The experimental pond was treated with Phoslock™ clay modified with lanthanum cations that irreversibly bind dissolved phosphorus in the water, and the pH was lowered to below 7.7 by adding molasses, which stimulates microbial growth. Despite these preventive measures, a bloom of bloom occurred at Barramundi Farm in Australia, resulting in the loss of all fish in the ponds. In response, a number of measures were taken to prevent similar incidents in the future [73]. To this end, an experimental manipulation of nutrients and pH was conducted in one of the ponds. The experimental pond was treated with Phoslock™ clay modified with lanthanum cations that irreversibly bind dissolved phosphorus in the water, and the pH was lowered to below 7.7 by adding molasses, which stimulates microbial growth. Despite these preventive measures, a bloom of P. parvum occurred in the culture ponds at water temperatures of 24 to 32 °C and salinities of 10 to 36 ppt, resulting in the death of all fish. Australia: Seger et al. [94]Australia: Seger et al. [73]
According to Guo et al. [95], citing numerous Chinese authors, there are three prymnesium species in China: According to Guo et al. [74], citing numerous Chinese authors, there are three prymnesium species in China: P. parvum, P. saltans, and P. papillarum. In 1963, a phytoplankton bloom caused by P. parvum resulted in the loss of 100,000 carp fry in a fish farm at the Liaoning Province Fishery College in Dalian. Since then, this alga has been found every year in different parts of China, such as Tianjin, the Ningxia Autonomous Region, Inner Mongolia, Shanxi and Zhejiang provinces, and the Tibet Autonomous Region. P. parvum thrives in coastal brackish water in Dalian, Tianjin, and Zhejiang and in saline, sulfate-bearing inland water in Ningxia, Inner Mongolia, and Shanxi. P. saltans, on the other hand, has been isolated from the coasts of Guangdong, Tianjin, and Ningxia and occurs in similar habitats and locations as Ningxia. P. papillarum has been isolated from the coast of Shandong Province. Chen and Zeng [96] described a new species in China that caused rotifers and copepods that fed on it to die within 2 to 4 days [95]. thrives in coastal brackish water in Dalian, Tianjin, and Zhejiang and in saline, sulfate-bearing inland water in Ningxia, Inner Mongolia, and Shanxi. P. saltans, on the other hand, has been isolated from the coasts of Guangdong, Tianjin, and Ningxia and occurs in similar habitats and locations as Ningxia. P. papillarum has been isolated from the coast of Shandong Province. Chen and Zeng [75] described a new species in China that caused rotifers and copepods that fed on it to die within 2 to 4 days [74]. China: Guo et al. [95]; Chen and Zeng [96]China: Guo et al. [74]; Chen and Zeng [75]
In 2007, an increase in the occurrence of the alternative algal species Prymnesium polylepis was detected during a marine monitoring program [97]. This species is considered the second most important ichthyotoxic haptophyte after was detected during a marine monitoring program [76]. This species is considered the second most important ichthyotoxic haptophyte after P. parvum. The peak of the extensive bloom occurred between March and May 2008 and was widespread in the southern, central, and northwestern Baltic Sea, with cell concentrations reaching up to 5 million cells per liter. At some sites, P. polylepis accounted for 30 to 90% of the total phytoplankton volume. However, in the northeastern Baltic Sea and the Gulf of Finland, P. polylepis was detected in low numbers. Larsson et al. [97] studied the effects of this extensive bloom on duck-billed birds, i.e., eiders (. The peak of the extensive bloom occurred between March and May 2008 and was widespread in the southern, central, and northwestern Baltic Sea, with cell concentrations reaching up to 5 million cells per liter. At some sites, P. polylepis accounted for 30 to 90% of the total phytoplankton volume. However, in the northeastern Baltic Sea and the Gulf of Finland, P. polylepis was detected in low numbers. Larsson et al. [76] studied the effects of this extensive bloom on duck-billed birds, i.e., eiders (Somateria mollissima), in the Baltic Sea. They observed a sharp decline in breeding eiders at 28 colonies in the southern and central Baltic Sea between 2007 and 2008. The authors argue that the intense spring bloom of P. polylepis affected the eiders’ main food source, i.e., mussels, at feeding sites in both toxic and non-toxic ways, which affected the body condition of adult female eiders and their breeding readiness. Denmark: Larsson et al. [97]Denmark: Larsson et al. [76]
In 1990, Lindholm and Virtanen reported a bloom of P. parvum in the Strait of Dragsfjaerd in Finland that resulted in a fish kill. The concentration of P. parvum reached a peak of 50,000 cells/mL. Chemical analyses conducted during the disappearance of the bloom showed a decrease in total phosphorus and total nitrogen levels and a decrease in chlorophyll a levels. Levels were about 50% lower in areas outside the strait where P. parvum was present in lower numbers. Live cells of P. parvum showed autofluorescence that could be of diagnostic value. Seven years later, in 1997, a brackish water lake in SW Finland, Vargsundet, was contaminated with algal toxins, resulting in high fish mortality. During this event, dense populations of Prymnesium sp. and the toxin-producing cyanobacterium Planktothrix agardhii were observed, mainly in separate layers [98]. were observed, mainly in separate layers [77]. Finland: Lindholm and Virtanen [98]Finland: Lindholm and Virtanen [77]
Great Britain is historically significant because it is the country where a case of P. parvum was first documented (according to Carter’s 1937 publication). More specifically, P. parvum habitats were found in a brackish pond near Bembridge on the Isle of Wight. In the 1960s, reports of the species’ occurrence surfaced in Hickling Broad, part of the Norfolk Broads. The Norfolk Broads, which consist of shallow brackish water created by centuries of peat extraction, are now used for recreational purposes and generate an estimated GBP 550 million in annual revenue for the local economy. According to Wagstaff et al. [99], habitats were found in a brackish pond near Bembridge on the Isle of Wight. In the 1960s, reports of the species’ occurrence surfaced in Hickling Broad, part of the Norfolk Broads. The Norfolk Broads, which consist of shallow brackish water created by centuries of peat extraction, are now used for recreational purposes and generate an estimated GBP 550 million in annual revenue for the local economy. According to Wagstaff et al. [78], P. parvum blooms have likely been present in the Norfolk Broads since the early 20th century. The frequency of blooms in the region is high, as evidenced by the toxic P. parvum bloom in Hickling Broad in 2015 that resulted in the death of thousands of fish. To contain the damage, 600,000 fish were manually relocated and rescued [100]. bloom in Hickling Broad in 2015 that resulted in the death of thousands of fish. To contain the damage, 600,000 fish were manually relocated and rescued [79]. Great Britain: Wagstaff et al. [99]; Wagstaff et al. [100];Great Britain: Wagstaff et al. [78]; Wagstaff et al. [79];
According to Shilo and Shilo [101], According to Shilo and Shilo [80], P. parvum first appeared in Israel in 1947 and then spread rapidly in brackish water areas, causing major problems for fish farming. The authors argue that the control of P. parvum can be achieved either by destroying the organism or its toxin. In 1947, Reich and Aschner discovered that ammonium sulfate had a destructive effect on P. parvum even at low concentrations and was not harmful to other life forms. Gordon and Colorni [102] reported a bloom of even at low concentrations and was not harmful to other life forms. Gordon and Colorni [81] reported a bloom of P. parvum in the Arava Valley in southern Israel that resulted in gradual death of ornamental fish, Poecilia sp. and koi. The toxic effect was due to changes in the water system, including higher temperatures, a tripling in salinity, and eutrophication, which favored the growth of P. parvum. Treatment with 10 ppm ammonium sulfate stopped the fish kill. Israel: Shilo and Shilo [101]; Gordon and Colorni [102]Israel: Shilo and Shilo [80]; Gordon and Colorni [81]
In 1990, a significant algal bloom and fish kill were observed in the Botshol Reserve in Utrecht, the Netherlands, which consists of two shallow lakes, ditches, and reed beds. The reserve was originally a system of clear lakes, but due to eutrophication, the water quality has deteriorated since the 1960s. Efforts were made to restore the reserve by reducing external phosphorus inputs. This resulted in a significant reduction in phosphorus levels in the lake water, an improvement in the light climate, and a change in the composition of phyto- and zooplankton. However, these measures also led to the appearance of P. parvum blooms [103]. blooms [82]. Netherlands: Rip et al. [103]Netherlands: Rip et al. [82]
In Norway, the occurrence of P. parvum has been documented along the entire west coast, from Oslofjord in the south to Spitsbergen in the north. However, blooms of the species have only been observed in the Sandsfjord fjord system, which is characterized by a permanent brackish water layer at a depth of 2–5 m and a summer salinity of 4–7 psu. The first recorded bloom of P. parvum in Sandsfjord occurred in late July 1989 and had severe consequences for local fish farms. According to Johnsen et al. [104], the bloom resulted in the death of 750 tons of Atlantic salmon and rainbow trout. In subsequent years, blooms of in Sandsfjord occurred in late July 1989 and had severe consequences for local fish farms. According to Johnsen et al. [83], the bloom resulted in the death of 750 tons of Atlantic salmon and rainbow trout. In subsequent years, blooms of P. parvum occurred repeatedly in July and August, resulting in losses to salmon farms. Due to the continued bloom, fish farmers finally decided to leave the area in 1995, which marked the end of the bloom. However, in 2005, an attempt to return to the region to farm fish resulted in another P. parvum bloom in 2007 and the loss of 135 tons of salmon. Norway: Johnsen et al. [104]Norway: Johnsen et al. [83]
The spread of the harmful P. parvum algae has caused major fish kills and financial losses in Texas and throughout the United States. According to Texas Parks and Wildlife agencies, fish kills in the upper Brazos River in 1981–1982 and in Red Bluff Reservoir in 1985 were likely caused by P. parvum, although this has not been confirmed. In 1985, P. parvum was confirmed as the cause of a 660 km fish kill in the Pecos River that resulted in the death of an estimated 110,000 fish. Between 1985 and 2000, P. parvum blooms caused fish kills in the Brazos, Colorado, and Rio Grande watersheds, killing an estimated 2.6 million fish. In the early 2000s, the rapid spread of P. parvum led to blooms in 15 other U.S. states, including Alabama, Arizona, and California. Now, the alga is present in all southern regions of the country and in some northern regions [77]. In 2001, a bloom of led to blooms in 15 other U.S. states, including Alabama, Arizona, and California. Now, the alga is present in all southern regions of the country and in some northern regions [56]. In 2001, a bloom of P. parvum caused significant damage to Texas fisheries. A winter bloom caused a massive fish kill in Lake Possum Kingdom and other reservoirs, as well as the death of over 5 million striped and hybrid perch fry in the Wichita River. In 2003, P. parvum invaded the Canadian River watershed and caused a minor fish kill. In subsequent years, more than 30 watersheds were affected by the alga. It is estimated that the P. parvum bloom caused the mortality of more than thirty-four million fish and caused tens of millions of dollars in financial losses [77]. Cases of bloom caused the mortality of more than thirty-four million fish and caused tens of millions of dollars in financial losses [56]. Cases of P. parvum have been reported throughout the decade 2011–2020 in several regions of the United States [105,106], including Brady Creek Reservoir (2012), Colorado City Reservoir (2016), Concho River (2019), Baylor Creek Reservoir (2009, 2012), Buffalo Springs Reservoir (2011–2012, 2014–2016), Balmorhea Revervoir (2010), Diversion Reservoir—Lake Diversion (2010–2016), and in Southern California, in Lake Forest and Lake Elsinore (2014). Detailed information can be found in the Nonindigenous Aquatic Species Database [105]. have been reported throughout the decade 2011–2020 in several regions of the United States [84][85], including Brady Creek Reservoir (2012), Colorado City Reservoir (2016), Concho River (2019), Baylor Creek Reservoir (2009, 2012), Buffalo Springs Reservoir (2011–2012, 2014–2016), Balmorhea Revervoir (2010), Diversion Reservoir—Lake Diversion (2010–2016), and in Southern California, in Lake Forest and Lake Elsinore (2014). Detailed information can be found in the Nonindigenous Aquatic Species Database [84]. United States: Roelke et al. [77]; Nonindigenous Aquatic Species Database [];

Caron [106]		United States: Roelke et al. [56]105; Nonindigenous Aquatic Species Database [84];

Caron [85]

References

  1. Baatrup, E. Structural and functional effects of heavy metals on the nervous system, including sense organs, of fish. Comp. Biochem. Physiol. Part C Comp. Pharmacol. 1991, 100, 253–257.
  2. Vilariño, N.; Louzao, M.C.; Abal, P.; Cagide, E.; Carrera, C.; Vieytes, M.R.; Botana, L.M. Human poisoning from marine toxins: Unknowns for optimal consumer protection. Toxins 2018, 10, 324.
  3. Arcand-Hoy, L.D.; Benson, W.H. Fish reproduction: An ecologically relevant indicator of endocrine disruption. Environ. Toxicol. Chem. Int. J. 1998, 17, 49–57.
  4. Liu, G.; Ke, M.; Fan, X.; Zhang, M.; Zhu, Y.; Lu, T.; Qian, H. Reproductive and endocrine-disrupting toxicity of Microcystis aeruginosa in female zebrafish. Chemosphere 2018, 192, 289–296.
  5. Rojas-Hucks, S.; Rodriguez-Jorquera, I.A.; Nimpstch, J.; Bahamonde, P.; Benavides, J.A.; Chiang, G.; Galbán-Malagón, C.J. South American National Contributions to Knowledge of the Effects of Endocrine Disrupting Chemicals in Wild Animals: Current and Future Directions. Toxics 2022, 10, 735.
  6. Segner, H.; Bailey, C.; Tafalla, C.; Bo, J. Immunotoxicity of xenobiotics in fish: A role for the aryl hydrocarbon receptor (AhR)? Int. J. Mol. Sci. 2021, 22, 9460.
  7. Segner, H.; Rehberger, K.; Bailey, C.; Bo, J. Assessing fish immunotoxicity by means of in vitro assays: Are we there yet? Front. Immunol. 2022, 13, 835767.
  8. Taslima, K.; Al-Emran, M.; Rahman, M.S.; Hasan, J.; Ferdous, Z.; Rohani, M.F.; Shahjahan, M. Impacts of heavy metals on early development, growth and reproduction of fish—A review. Toxicol. Rep. 2022, 9, 858–868.
  9. Dao, H.V.; Uesugi, A.; Uchida, H.; Watanabe, R.; Matsushima, R.; Lim, Z.F.; Suzuki, T. Identification of fish species and toxins implicated in a snapper food poisoning event in Sabah, Malaysia, 2017. Toxins 2021, 13, 657.
  10. EPA. Toxics in the Food Web; Environmental Protection Agency: Washington, DC, USA, 2021.
  11. Bhuyan, M.S. Effects of microplastics on fish and in human health. Front. Environ. Sci. 2022, 10, 250.
  12. Allaf, M.M.; Trick, C.G. Yeast Cell as a Bio-Model for Measuring the Toxicity of Fish-Killing Flagellates. Toxins 2021, 13, 821.
  13. Sharma, L.; Siedlewicz, G.; Pazdro, K. The toxic effects of antibiotics on freshwater and marine photosynthetic microorganisms: State of the art. Plants 2021, 10, 591.
  14. Keena, M.; Meehan, M.; Scherer, T. Environmental Implications of Excess Fertilizer and Manure on Water Quality; North Dakota State University: Fargo, ND, USA, 2022.
  15. Hargreaves, J.A.; Tucker, C.S. Managing Ammonia in Fish Ponds; Southern Regional Aquaculture Center: Stoneville, NC, USA, 2004; Volume 4603.
  16. Camargo, J.A.; Alonso, Á. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: A global assessment. Environ. Int. 2006, 32, 831–849.
  17. Nicholas, W.; Brye, B.A. Experience with Heavy Metals in the Tennessee Valley Authority System: Proceedings of the International Conference Held in Nashville, Tennessee, USA, December 1973; Pergamon Press: London, UK, 1973.
  18. Bu-Olayan, A.H.; Thomas, B.V. Validating mercury levels in catfish Netuma thalassina (Rüppell, 1837) during and aftermath ‘fish kill’in Kuwait Bay. Iran. J. Fish. Sci. 2020, 19, 3151–3159.
  19. Zaynab, M.; Al-Yahyai, R.; Ameen, A.; Sharif, Y.; Ali, L.; Fatima, M.; Li, S. Health and environmental effects of heavy metals. J. King Saud Univ. Sci. 2022, 34, 101653.
  20. EPA. Polychlorinated Biphenyls (PCBs) Update: Impact on Fish Advisories; Environmental Protection Agency: Washington, DC, USA, 1999.
  21. Duke, T.W.; Lowe, J.I.; Wilson, A.J. A polychlorinated biphenyl (Aroclor 1254) in the water, sediment, and biota of escambia bay, Florida. Bull. Environ. Contam. Toxicol. 1970, 5, 171–180.
  22. Nestel, H.; Budd, J. Chronic oral exposure of rainbow trout (Salmo gairdneri) to a polychlorinated biphenyl (Aroclor 1254): Pathological effects. Can. J. Comp. Med. 1975, 39, 208.
  23. Henry, T.B. Ecotoxicology of polychlorinated biphenyls in fish—A critical review. Crit. Rev. Toxicol. 2015, 45, 643–661.
  24. Eisler, R.; Wiemeyer, S.N. Cyanide hazards to plants and animals from gold mining and related water issues. Rev. Environ. Contam. Toxicol. 2004, 183, 21–54.
  25. National Research Council Committee. Oil in the Sea: Inputs, Fates, and Effects; National Academies Press: Washington, DC, USA, 2003.
  26. Barron, M.G.; Vivian, D.N.; Heintz, R.A.; Yim, U.H. Long-term ecological impacts from oil spills: Comparison of Exxon Valdez, Hebei Spirit, and Deepwater Horizon. Environ. Sci. Technol. 2020, 54, 6456–6467.
  27. Aktar, W.; Sengupta, D.; Chowdhury, A. Impact of pesticides use in agriculture: Their benefits and hazards. Interdiscip. Toxicol. 2009, 2, 1.
  28. EPA. Protecting Water Quality from Agricultural Runoff; Environmental Protection Agency: Washington, DC, USA, 2005.
  29. U.S. National Office for Harmful Algal Blooms. Examples of Socioeconomic Impacts. Harmful Algae. Available online: https://hab.whoi.edu/impacts/impacts-socioeconomic/ (accessed on 20 February 2023).
  30. Sha, J.; Xiong, H.; Li, C.; Lu, Z.; Zhang, J.; Zhong, H.; Yan, B. Harmful algal blooms and their eco-environmental indication. Chemosphere 2021, 274, 129912.
  31. Burkholder, J.M. Harmful algal blooms. In Encyclopedia of Inland Waters; Cary Institute of Ecosystem Studies Millbrook: New York, NY, USA, 2009; Volume 1, pp. 264–285.
  32. Larson, S.J.; Capel, P.D.; Majewski, M.S. Pesticides in Surface Waters: Distribution, Trends, and Governing Factors; CRC Press: Boca Raton, FL, USA, 2019; p. 278.
  33. Rosseland, B.O.; Blakar, I.A.; Bulger, A.; Kroglund, F.; Kvellstad, A.; Lydersen, E.; Vogt, R. The mixing zone between limed and acidic river waters: Complex aluminium chemistry and extreme toxicity for salmonids. Environ. Pollut. 1992, 78, 3–8.
  34. Rask, M.; Järvinen, M.; Kuoppamäki, K.; Pöysä, H. Limnological responses to the collapse of the perch population in a small lake. Ann. Zool. Fenn. 1996, 1, 517–524.
  35. Poléo, A.B. Aluminium polymerization—A mechanism of acute toxicity of aqueous aluminium to fish. Aquat. Toxicol. 1995, 31, 347–356.
  36. Francis-Floyd, R.; Riggs, A.; Philips, E. A Beginner’s Guide to Water Management—Fish Kills; University of Florida, Institute of Food and Agricultural Sciences: Gainesville, FL, USA, 2004.
  37. DiPinto, L.; Penn, T.; Iliff, J.; Peterson, C. Determining the Scale of Restoration for a Fish Kill in the Alafia River, FLORIDA; American Petroleum Institute: Washington, DC, USA, 2001.
  38. Khalidi-idrissi, A.; Madinzi, A.; Anouzla, A.; Pala, A.; Mouhir, L.; Kadmi, Y.; Souabi, S. Recent advances in the biological treatment of wastewater rich in emerging pollutants produced by pharmaceutical industrial discharges. Int. J. Environ. Sci. Technol. 2023, 20, 1–22.
  39. Cormier, S.M.; Suter, G.W.; Norton, S.B. Causal characteristics for ecoepidemiology. Hum. Ecol. Risk Assess. 2010, 16, 53–73.
  40. Fujawa, E. 100 Years of Contamination: The White River Fish Kills of 1896 and 1999. Available online: https://www.class900indy.com/post/100-years-of-contamination-the-white-river-fish-kills-of-1896-and-1999 (accessed on 17 May 2023).
  41. Bowman, S. 113 Tons of Dead Fish: Indiana’s Worst Environmental Disaster, 20 Years Later. Available online: https://www.indystar.com/in-depth/news/environment/2019/12/19/guide-corp-s-toxic-discharge-killed-millions-fish-white-river/4385458002/ (accessed on 17 May 2023).
  42. Thornhill Law Firm. Temple-Inland Pearl River Paper Mill Spill. Available online: https://www.thornhilllawfirm.com/temple-inland-pearl-river-paper-mill-spill.html (accessed on 17 May 2023).
  43. Mother Earth News. Manure Spills: The Environmental Damage We Don’t Hear About. Available online: https://www.motherearthnews.com/sustainable-living/nature-and-environment/environmental-damage-from-spills-ze0z1411zdeh/ (accessed on 17 May 2023).
  44. Kamana, L. Trapped Fish, Just One of Many Environmental Impacts Left by Flood. Available online: https://midmichigannow.com/news/local/trapped-fish-just-one-of-many-environmental-impacts-left-by-flood (accessed on 17 May 2023).
  45. U.S. Fish and Wildlife Service. Tittabawassee River—Saginaw River & Bay Natural Resource Trustee Councils Draft Supplemental Restoration Plan and Environmental Assessment. Available online: https://www.fws.gov/sites/default/files/documents/nrdar-draft-supplemental%20restoration%20plan-environmental%20assessment-2023-tittabawassee%20saginaw%20river.pdf (accessed on 17 May 2023).
  46. Wilkerson, I. Tainting of Fish Feared after Michigan Floods. Available online: https://www.nytimes.com/1986/09/24/us/tainting-of-fish-feared-after-michigan-floods.html (accessed on 17 May 2023).
  47. Public Sector Consultants, Inc. Measures of Success: Addressing Environmental Impairments in the Saginaw River and Saginaw Bay. Available online: https://www.baycounty-mi.gov/Docs/EACD/Measures%20of%20Success%20-%20Saginaw%20River%20and%20Bay.pdf (accessed on 17 May 2023).
  48. Hartig, J. Roller Coaster: Michigan’s Long History with Environmental Contamination. Available online: https://www.greatlakesnow.org/2020/06/michigan-history-environmental-contamination/ (accessed on 17 May 2023).
  49. Magaña, H.A.; Contreras, C.; Villareal, T.A. A historical assessment of Karenia brevis in the western Gulf of Mexico. Harmful Algae 2003, 2, 163–171.
  50. Castle, K.T.; Flewelling, L.J.; Bryan, J.; Kramer, A.; Lindsay, J.; Nevada, C.; Landsberg, J.H. Coyote (Canis latrans) and domestic dog (Canis familiaris) mortality and morbidity due to a Karenia brevis red tide in the Gulf of Mexico. J. Wildl. Dis. 2013, 49, 955–964.
  51. Butler, N.; Carlisle, J.C.; Linville, R.; Washburn, B. Microcystins. A Brief Overview of Their Toxicity and Effects, with Special Reference to Fish, Wildlife, and Livestock; Office of Environmental Health Hazard Assessment: Sacramento, CA, USA, 2009.
  52. Ferrão-Filho, A.D.; Kozlowsky-Suzuki, B. Cyanotoxins: Bioaccumulation and effects on aquatic animals. Mar. Drugs 2011, 9, 2729–2772.
  53. Kang, Y.; Gobler, C.J. The brown tide algae, Aureococcus anophagefferens and Aureoumbra lagunensis (Pelagophyceae), allelopathically inhibit the growth of competing microalgae during harmful algal blooms. Limnol. Oceanogr. 2018, 63, 985–1003.
  54. Watson, S.B.; Whitton, B.A.; Higgins, S.N.; Paerl, H.W.; Brooks, B.W.; Wehr, J.D. Harmful algal blooms. In Freshwater Algae of North America; Academic Press: Cambridge, MA, USA, 2015; pp. 873–920.
  55. Roelke, D.L.; Manning, S.R. Harmful Algal Species Fact Sheet: Prymnesium parvum (Carter) “Golden Algae”. Harmful Algal Blooms: A Compendium Desk Reference, 1st ed.; Wiley: Hoboken, NJ, USA, 2018; pp. 629–632.
  56. Roelke, D.L.; Barkoh, A.; Brooks, B.W.; Grover, J.P.; Hambright, K.D.; LaClaire, J.W.; Patino, R. A chronicle of a killer alga in the west: Ecology, assessment, and management of Prymnesium parvum blooms. Hydrobiologia 2016, 764, 29–50.
  57. Wagstaff, B.A.; Hems, E.S.; Rejzek, M.; Pratscher, J.; Brooks, E.; Kuhaudomlarp, S.; Field, R.A. Insights into toxic Prymnesium parvum blooms: The role of sugars and algal viruses. Biochem. Soc. Trans. 2018, 46, 413–421.
  58. Anderson, D.M.; Burkholder, J.M.; Cochlan, W.P.; Glibert, P.M.; Gobler, C.J.; Heil, C.A.; Vargo, G.A. Harmful algal blooms and eutrophication: Examining linkages from selected coastal regions of the United States. Harmful Algae 2008, 8, 39–53.
  59. Heisler, J.; Glibert, P.M.; Burkholder, J.M.; Anderson, D.M.; Cochlan, W.; Dennison, W.C.; Suddleson, M. Eutrophication and harmful algal blooms: A scientific consensus. Harmful Algae 2008, 8, 3–13.
  60. CDC. Harmful Algal Bloom—Associated Illnesses. Available online: https://www.cdc.gov/habs/environment.html (accessed on 26 April 2023).
  61. EPA. Harmful Algal Blooms. Available online: https://www.epa.gov/nutrientpollution/harmful-algal-blooms (accessed on 26 April 2023).
  62. NOAA. National Oceanic and Atmospheric Administration What Is Eutrophication? Available online: https://oceanservice.noaa.gov/facts/eutrophication.html (accessed on 26 April 2023).
  63. Kangur, K.; Kangur, A.; Kangur, P.; Laugaste, R. Fish kill in Lake Peipsi in summer 2002 as a synergistic effect of a cyanobacterial bloom, high temperature, and low water level. Proc. Estonian Acad. Sci. Biol. Ecol. 2005, 54, 67–80.
  64. Carter, N. New or interesting algae from brackish water. Arch. Protistenk. 1937, 90, 1–68.
  65. Igarashi, T.; Satake, M.; Yasumoto, T. Prymnesin-2: A potent ichthyotoxic and hemolytic glycoside isolated from the red tide alga Prymnesium parvum. J. Am. Chem. Soc. 1996, 118, 479–480.
  66. Larsen, A. Prymnesium parvum and P. patelliferum (Haptophyta)—One species. Phycologia 1999, 38, 541–543.
  67. Edvardsen, B.; Eikrem, W.; Throndsen, J.; Saez, A.G.; Probert, I.; Medlin, L.K. Ribosomal DNA phylogenies and a morphological revision provide the basis for a revised taxonomy of the Prymnesiales (Haptophyta). Eur. J. Phycol. 2011, 46, 202–228.
  68. Manton, I.; Leedale, G.F. Observations on the fine structure of Prymnesium parvum Carter. Archiv. Mikrobiol. 1963, 45, 285–303.
  69. Manton, I. Observations with the electron microscope on the division cycle in the flagellate Prymnesium parvum Carter. J. Royal Microsc. Soc. 1964, 83, 317–325.
  70. Moestrup, Ø.; Thomsen, H.A. Taxonomy of toxic haptophytes (prymnesiophytes). Man. Harmful Mar. Microalgae 2003, 33, 433.
  71. Seoane, S.; Eikrem, W.; Pienaar, R.; Edvardsen, B. Chrysochromulina palpebralis sp. nov. (Prymnesiophyceae): A haptophyte, possessing two alternative morphologies. Phycologia 2009, 48, 165–176.
  72. González, A.; Broce, K.; Fábrega-Duque, J.; Tejedor-Flores, N.; Young, K. Identification and monitoring of microalgal genera potentially capable of forming harmful algal blooms in Punta Galeta, Panama. Air Soil Water Res. 2019, 12, 1178622119872769.
  73. Seger, A.; Dorantes-Aranda, J.J.; Müller, M.N.; Body, A.; Peristyy, A.; Place, A.R.; Hallegraeff, G. Mitigating fish-killing Prymnesium parvum algal blooms in aquaculture ponds with clay: The importance of pH and clay type. J. Mar. Sci. Eng. 2015, 3, 154–174.
  74. Guo, M.; Harrison, P.J.; Taylor, F.J.R. Fish kills related to Prymnesium parvum N. Carter (Haptophyta) in the People’s Republic of China. J. Appl. Phycol. 1996, 8, 111–117.
  75. Chen, S.F.; Zeng, C.K. Two species of Prymnesium from the North China. Oceanol. Limnol. Sin. 1986, 17, 394–399.
  76. Larsson, K.; Hajdu, S.; Kilpi, M.; Larsson, R.; Leito, A.; Lyngs, P. Effects of an extensive Prymnesium polylepis bloom on breeding eiders in the Baltic Sea. J. Sea Res. 2014, 88, 21–28.
  77. Lindholm, T.; Virtanen, T. A bloom of Prymnesium parvum Carter in a small coastal inlet in Dragsfjärd, southwestern Finland. Environ. Toxicol. Water Qual. 1992, 7, 165–170.
  78. Wagstaff, B.A.; Pratscher, J.; Rivera, P.P.L.; Hems, E.S.; Brooks, E.; Rejzek, M.; Field, R.A. Assessing the toxicity and mitigating the impact of harmful Prymnesium blooms in eutrophic waters of the Norfolk Broads. Environ. Sci. Technol. 2021, 55, 16538–16551.
  79. Wagstaff, B.A.; Pratscher, J.; Rivera, P.P.L.; Hems, E.S.; Brooks, E.; Rejzek, M.; Field, R.A. Dissecting the toxicity and mitigating the impact of harmful Prymnesium blooms in the UK waters of the Norfolk Broads. bioRxiv Electron. J. 2020, 1, 2020–2023.
  80. Shilo, M.; Shilo, M. Conditions which determine the efficiency of ammonium sulphate in the control of Prymnesium parvum in fish breeding ponds. Appl. Microbiol. 1953, 1, 330–333.
  81. Gordon, N.; Colorni, A. Prymnesium parvum, an Ichthyotoxic Alga in an Ornamental Fish Farm in Southern Israel. Israeli J. Aquacult. Bamidgeh 2008, 60, 5–8.
  82. Rip, W.J.; Everards, K.; Houwers, A. Restoration of Botshol (The Netherlands) by reduction of external nutrient load: The effects on physico-chemical conditions, plankton and sessile diatoms. Hydrobiol. Bull. 1992, 25, 275–286.
  83. Johnsen, T.M.; Eikrem, W.; Olseng, C.D.; Tollefsen, K.E.; Bjerknes, V. Prymnesium parvum: The Norwegian Experience 1. JAWRA J. Am. Water Resour. Assoc. 2010, 46, 6–13.
  84. U.S. Geological Survey. Nonindigenous Aquatic Species Database. Available online: https://nas.er.usgs.gov/queries/collectioninfo.aspx?SpeciesID=3234 (accessed on 25 April 2023).
  85. Caron, D.A. Temporal and Geographic Progression of Prymnesium parvum (the ‘Golden Alga’) in the Southwestern United States; Department of Biologial Sciences, University of Southern California: Los Angeles, CA, USA, 2017.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
ScholarVision Creations
Feedback