Toxins and Toxins Secreted by Algal Bloom Habitats: History
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Contributor:
Janusz Sobieraj
,
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 [1]; (3) damage the liver, kidneys, and other organs, leading to organ failure and death [2]; (4) disrupt the hormonal system, leading to reproductive failure [3][4][5]; (5) disrupt the immune system and make fish more susceptible to disease [6][7]; (6) impair fish growth and development, leading to abnormal growth or even death [8]; and (7) accumulate in fish tissues and can be passed through the food chain, making fish unsafe for human consumption [9]. It is important to know that toxic substances can come from many sources, including industrial pollution, agricultural runoff [10][11], and even naturally occurring toxins produced by certain species of algae or bacteria [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 [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 [15][16]. (2) Heavy metals such as lead, mercury [17][18], and cadmium can be toxic to fish, and high concentrations of these compounds can cause mass fish kills [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 [20], leading to massive fish die-offs [21][22][23]. (4) Cyanide, which can also be toxic to fish and leads to massive fish kills [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 [25][26]. (6) Pesticides—toxic to fish and cause massive fish kills [27]. Pesticides can enter waterways through agricultural runoff and other forms of pollution [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 [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. [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 [33], i.e., harmful interactions between acid, calcium, and labile aluminum at certain concentrations [34] or chemical interactions with complex polymeric aluminum salts [35]. Rosseland et al. [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. [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) [36] and contributing to the mass mortality of more than one million fish [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 [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 [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 [40]. The investigation traced back to Guide Corp, a manufacturer of automotive lamps that had discharged toxic waste into the river [41]. In 2011, the Temple-Inland paper mill in Bogalusa, Louisiana, discharged chemicals into the Pearl River, causing a massive fish kill [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 [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) [44]. In 2023, hazardous materials were released into the Tittabawassee River and transported downstream to the Saginaw River and Bay [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) [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 [47]. In 2017, PFAS contamination of drinking water and fish was discovered in the Huron River in southeast Michigan [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 research. 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) [49][50], cyanobacterial blooms [51][52], brown tide (Aureococcus anophagefferens) [53], diatom blooms [54], and P. parvum (also known as golden alga) [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 [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. [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 [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 [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 [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 [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 [64]. Moreover, the prymnesins were first isolated only in the late 20th century (1995 to be precise) [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 [66] and Edvardsen et al. [67]. Furthermore, P. parvum (N. Carter) was well-documented and described in the 1960s by Manton and Leedale [68] and Manton [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 [70][71] (see Figure 1).
Toxins 15 00403 g001 550
Figure 1. P. parvum (N. Carter 1937) [64].
P. parvum is a species of golden alga that has flagella and chloroplasts for photosynthesis [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 [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 research 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 [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. [73]
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 [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. [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 [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. [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. [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 [77]. 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. [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 [79]. Great Britain: Wagstaff et al. [78]; Wagstaff et al. [79];
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 [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 [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 [82]. 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. [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. [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 [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 [56]. Cases of P. parvum 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. [56]; Nonindigenous Aquatic Species Database [84];
Caron [85]

This entry is adapted from the peer-reviewed paper 10.3390/toxins15060403

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