1. Introduction
Algae are ancient and diverse eukaryotes (i.e., organisms with a membrane-bound nucleus) with hundreds of thousands of species globally (Wehr 2015). Cyanobacteria are Earth’s oldest known oxygen-producing organisms (Schopf 2002), and their proliferation during the Precambrian era is largely responsible for Earth’s oxygen-enriched atmosphere and the subsequent evolution of higher plant and animal life (Knoll 2015). Cyanobacteria often are referred to as “blue-green algae,” but they are not algae. They are unicellular, photosynthetic prokaryotes (i.e., organisms without a nucleus) and have the ability to synthesize chlorophyll-a and form the pigment phycocyanin (Whitton and Potts 2002). Under certain conditions, high concentrations of this pigment lead to the bluish color of the organism (Whitton and Potts 2002)—hence the misnomer “blue-green algae” (Fig. 1).
Image of a freshwater harmful algal bloom acquired from NASA’s Landsat-5 satellite on 5 Oct 2011. The green filaments show a portion of an extensive bloom of primarily Microcystis aeruginosa that spread across the western waters of Lake Erie. Credit: NASA (2011).
Citation: Earth Interactions 28, 1; 10.1175/EI-D-23-0008.1
Phytoplankton, a large group of photosynthetic microorganisms that drift in water, contain both prokaryotic bacteria (e.g., cyanobacteria) and eukaryotic algae (Mur et al. 1999). In fresh, estuarine, or marine waters, unusual proliferation of these phytoplankton are referred to as “blooms,” with toxic blooms generally termed “harmful algal blooms” (HABs). Not all blooms are toxic, but a bloom can be harmful without producing toxins, such as by blocking light to other organisms or depleting oxygen in the water. Indiscriminate use of the term HAB is often based on qualitative knowledge rather than quantitative ecological studies (Smayda 1997). Blooms caused by known cyanobacteria taxa also have been called cyanoHABs (CHABs). Related names include “red tide” or “brown tide,” which occur in marine systems and typically are associated with algae species. For our purposes, we use the terms “harmful algal bloom” or “HAB” interchangeably to include both algae and cyanobacteria blooms that have adverse effects to humans and both wild and domestic animals.
Algae and cyanobacteria developed evolutionary diversity and effective strategies for dominance and survival in aquatic environments, making them resilient in systems undergoing human-induced environmental change (Huisman and Hulot 2005). In particular, nutrient overenrichment, particularly of nitrogen and phosphorus, leads to eutrophication (i.e., excessive photosynthetic growth of phytoplankton or aquatic plants) that favors periodic dominance of cyanobacteria and algae in freshwater systems (Paerl and Huisman 2009). This overenrichment is associated with urban, agricultural, and industrial development and expansion. Changes in nutrient sources and amounts from land, air, and water have been most evident during the past few decades with substantial population growth, but also are associated with other ecosystem changes related to alterations in climate (Glibert and Burford 2017).
Harmful algal blooms impair water quality, are potentially life-threatening to humans, and have caused fatalities to wildlife, livestock, and pets (Wood 2016). Although historical records dating back to the early nineteenth century showed that HABs have killed animals and sickened humans, HABs remained underdocumented (Brooks et al. 2016). Phytoplankton-eating fish and zooplankton typically do not eat cyanobacteria and, hence, are rarely affected by blooms (Chapra et al. 2017). Harmful algal blooms also reduce water clarity and, thus, the optimal aquatic habitat for other species (Coffey et al. 2019). In some cases, HAB material washes ashore as unattractive surface scums, decomposes, and creates foul odors (Coffey et al. 2019). Although the primary driver of HABs is excessive nutrients carried to water bodies from agricultural and urban environments, climate change stressors, such as warmer air and water temperatures and more intense precipitation extremes (i.e., drought and heavy downpours), influence the frequency and severity of harmful algal blooms.
The adverse impacts of HABs required legislative action to address the problem. The proliferation of harmful algal blooms and the severity of the threats they pose was highlighted by the 105th Congress of the United States, resulting in the passage of the Harmful Algal Bloom and Hypoxia Research and Control Act of 1998 with amendments in 2004 and 2014 and reaffirmed in 2017 (Nelson et al. 2019). The Act established an interagency task force with the focus to develop a national assessment of harmful algal blooms. Funding was designated to the National Oceanic and Atmospheric Administration (NOAA), with early research primarily focused on marine or coastal habitats. The 2004 reauthorization of Harmful Algal Bloom and Hypoxia Research and Control Act added a focus on the Great Lakes region, increasing research efforts on freshwater HABs (Ehlers et al. 2004). Yet, there remained limited research on other freshwater habitats such as inland lakes and reservoirs outside of the Great Lakes. There is even less research directed to waters on tribal reservations or shared jurisdictional water bodies that have cultural significance to a tribe. Tribes are sovereign and have a government-to-government relationship with federal agencies, but there are no funds through this legislation that are specific for tribes.
In this review, we synthesize current knowledge of climate change stressors on the occurrence and intensity of HABs, primarily cyanobacteria blooms in freshwater systems, and the consequences of these changes to humans, wildlife, and domesticated animals. Our intent is to focus the discussion to inland water bodies of the United States apart from the Great Lakes. This review presents examples of monitoring and reporting efforts by states, tribes, and federal agencies, primarily focused on inland freshwater HABs, which are projected to increase substantially with warming temperatures and more frequent drought conditions.
2. Relationship of HABs and climate change
Chemical, biological, and physical factors affect water quality, and humans can influence these factors greatly (Codd 2000). For example, the use of phosphorus and nitrogen in artificial fertilizer for large-scale agriculture increased with the population boom after World War II. The nonpoint source pollution caused by industrialized farming practices and carried into streams by rainfall runoff led to impaired water quality (Brett et al. 2005; Carpenter et al. 1998). Increases in nitrogen and phosphorus usage were shown to be a significant contributing factor in eutrophication, leading to an increase in both marine and freshwater HABs (Glibert et al. 2005).
The first efforts to clean the nation’s water bodies after the enactment of the Clean Water Act of 1972 were focused on point-source pollution, which is effluent released via a pipe from industrial wastewater or sewage treatment plants (Bonsdorff 2021). The Clean Water Act required pretreatment of effluent from these sources, reducing the adverse impact from industrial releases (EPA 2013). Nonpoint sources of pollution, however, enter water bodies from runoff over the landscape and from deposition from the airshed, making them harder to control or treat. As a result, freshwater harmful algal blooms are increasing in frequency and intensity from this nutrient enrichment (Glibert et al. 2005; Paerl and Paul 2012). In addition, the global increase in human population and urbanization are associated with eutrophication, causing species’ shifts in the phytoplankton community whereby cyanobacteria begin to dominate (Anderson et al. 2002; Brett et al. 2005; Dale et al. 2006).
There are signs that climate change is exacerbating this anthropogenic eutrophication, leading to conditions that favor increased frequency, severity, and range expansion of freshwater HABs in the United States (Glibert 2020; Smucker et al. 2021; Wells et al. 2020). Higher concentrations of atmospheric carbon dioxide—the main driver of climate change—favor growth of cyanobacteria on the surface of water bodies through increased photosynthesis (i.e., direct access to more carbon dioxide) (Paerl and Paul 2012; Raven et al. 2020). Acidification of water bodies also results from an increase in atmospheric carbon dioxide that dissolves into surface waters, adding additional stress to aquatic species that cohabit lakes with HABs (Griffith and Gobler 2020). However, the process of photosynthesis consumes carbon dioxide during a bloom and the pH increases, providing a competitive advantage to cyanobacteria (Bullerjahn et al. 2016; Krausfeldt et al. 2019). In addition, increased water temperatures, increased length of stratification in lakes, and changes in water quality because of heavier rainfall and drought are consequences of climate change and affect the growth of phytoplankton (Tewari 2022). In most cases, multiple stressors (e.g., drought, hot temperatures, weak winds, clear skies, and high nitrogen levels) interact and can lead to nonlinear effects whereby outcomes are more or less severe than one would expect additively (Griffith and Gobler 2020; Jöhnk et al. 2008)
a. Temperature and stratification
The global-average temperature is increasing, leading to warming in most regions during most times of the year (IPCC 2021) and this warming affects the prevalence, timing, and toxin production of harmful algal blooms. All algae and cyanobacteria species have a temperature range conducive for optimal growth, and this range varies among species (Wells et al. 2020). Changes in air and water temperatures affect the habitat for algae and cyanobacteria, with many cyanobacteria species preferring warmer temperatures (Glibert 2020). Temperatures that favor success for cyanobacteria growth and proliferation are in excess of 25°C (Paerl and Huisman 2009). The rate of cellular processes for phytoplankton, as a group, increase with warmer temperatures, with a maximum range between 25° and 40°C (Paerl and Huisman 2009; Robarts and Zohary 1987). More available light and a lack of water turbulence (e.g., due to calm winds) also contribute to phytoplankton growth (Paerl et al. 2001). As cyanobacteria grow, they strongly absorb incoming solar energy, causing a local warming of water temperatures—a positive feedback that enhances growth (Paulsen et al. 2018). Also, as temperatures warm, nutrient loads do not need to be as high for cyanobacteria to dominate phytoplankton growth in lakes (Kosten et al. 2012). These factors change the physical characteristics of aquatic environments and, thus, the growth success of cyanobacteria species (Jöhnk et al. 2008; O’Neil et al. 2012).
As ambient air temperatures increase with climate change, surface-water temperatures warm, causing changes in the physical structure of the water column in lakes and reservoirs. The heat exchange at the air–water surface, combined with surfaces winds inducing turbulence on the water, affects stratification (Woolway et al. 2021). Freshwater stratification results from water density changes as temperatures change; water is most dense at almost 4°C (Huttula 2012). The relationship between temperature and water density drives the process of a lake to stratify into layers during the warm season, with warm, well-mixed water on top, a relatively deep and stable thermocline in the middle, and the coldest water on bottom (Jørgensen et al. 2012). Increasing temperatures reduce the density of the surface waters, strengthening the vertical stratification (Paerl and Huisman 2009).
Some cyanobacteria species form gas vesicles that provide them with the ability to regulate their buoyancy (i.e., vertical position) in the stratified water column. Enhanced stratification allows cyanobacteria the ability to form gas vesicles to outcompete phytoplankton that cannot adjust their buoyancy (Huisman and Hulot 2005; Paerl and Huisman 2009). As near-surface temperatures increase, the water column becomes more stable and sinking rates for taxa without gas vesicles increase, thus interfering with the ability of these phytoplankton to photosynthesize (Glibert 2020). Hence, warmer conditions favor vesicle-producing cyanobacteria to form blooms through their ability to position themselves within their optimum temperature range and block sunlight needed for photosynthesis for other competing phytoplankton deeper in the water column (O’Neil et al. 2012; Visser et al. 2016).
With climate change, seasonal patterns are shifting to both an earlier onset of warm temperatures (that triggers lake stratification) in the spring and a later breakup of stratification in autumn, extending the period when cyanobacteria can thrive (Wagner and Adrian 2009; Wells et al. 2015; Woolway et al. 2021). Woolway et al. (2021), for example, used several lake models from the Inter-Sectoral Impact Model Intercomparison Project to calculate the onset and breakup of summer stratification (defined as a density difference of 0.1 kg m−3 between surface and bottom waters) in Northern Hemisphere lakes. After developing a base-period climatology using historical data from 1970 to 1999, the models were used to simulate annual changes (from the base period) in stratification onset and breakup from 1901 to 2099 using output from multiple global climate models and future scenarios. Changes during the historical period were verified with observational data from in situ studies for several well-monitored lakes with long periods of record. Results indicated that there had been considerable change in stratification phenology. For example, onset and breakup of stratification at Blelham Tarn (United Kingdom) were respectively 24 days earlier and 18 days later from 1963 to 2017. Stratification onset for Lakes Huron, Michigan, and Superior (United States–Canada) occurred 3.5 ± 2.2 days per decade earlier from 1980 to 2019 (Woolway et al. 2021). Lengthening of the stratification season can result in the depletion of oxygen (Jane et al. 2023), affecting the lake sediments that, in turn, impacts HAB growth (Tewari 2022).
The toxin quota of freshwater HABs also may be affected by temperature, but study results conflict on whether the toxin quota increases or decreases when temperatures increase. Results of a study in western Ohio that included both in situ and laboratory experiments indicated that the biomass of Planktothrix agardhii–dominated blooms increased as temperatures warmed to 18°C and declined in warmer temperatures while the release of microcystin toxins from the bloom peaked at 20°–25°C (Walls et al. 2018). Peng et al. (2018) found that growth rates of Microcystis aeruginosa—a species common to freshwater cyanobacterial blooms—were slower at cooler temperatures but nitrogen concentration had no effect on toxin production. In this case, the Microcystin toxin quota peaked at temperatures below the optimum growth rate of about 18°–20°C. Although temperature is a key factor in the growth of HABs, it also works in association with other factors, such as level of nutrient input. For example, in the same laboratory experiments, Peng et al. (2018) noted that at cooler temperatures nitrogen concentration did not affect toxin levels, but at warmer temperatures toxin production increased as the nitrogen concentration decreased. In a study of four northeastern U.S. lakes, the growth of cyanobacteria blooms of toxic Microcystis species varied based on both increasing temperature and enrichment of nitrogen and phosphorus (Davis et al. 2009).
b. Precipitation extremes
Water quality in both still (lotic) and rapidly moving (lentic) freshwater systems relies on complex interactions of physical, chemical, and biological factors that are affected by rainfall events and the subsequent movement of particulates, such as pollutants, into the water body (Leopold 1997). Climate change is impacting precipitation patterns and the intensity, duration, frequency, and timing of rainfall events (IPCC 2021). The subsequent changes in runoff can favor conditions that later enhance cyanobacteria dominance and promote HABs (Moore et al. 2008; Paerl et al. 2001; Paerl and Huisman 2009; Paerl and Paul 2012; Wells et al. 2015). During and after a heavy rainfall event, sediment from the watershed carries pollutants and nutrients to a receiving water body in the catchment area and, as water velocity slows, the pollutant- and nutrient-laden sediments are deposited into the water body (Gordon et al. 2008; Hauer and Lamberti 2006; Leopold 1992). Nitrogen, phosphorus, and other nutrients also are deposited into surface waters directly from the precipitation (Clark et al. 2000), so changing rainfall amount and patterns will alter surface-water chemistry needed for cyanobacterial growth. Water conductivity reduces after rainfall, especially if the rain event was preceded by drought (Reichwaldt and Ghadouani 2012). Depending on the rainfall timing and intensity, conductivity can remain high enough to limit other phytoplankton species but, with the added nutrient pulse, can enhance cyanobacteria growth.
For locations or seasons with frequent rainfall and resulting high values of discharge into lakes and reservoirs, cyanobacteria biomass tends to be reduced as turbulence and mixing temporarily prevents blooms, then will increase as discharge rates become lower over time (Srifa et al. 2016). Long periods of dry conditions, however, interrupted occasionally by heavy rainfall events promote cyanobacteria growth, allowing cyanobacteria to dominate the phytoplankton population (Paerl et al. 2016; Paerl and Huisman 2009; Paerl and Otten 2013; Paerl and Paul 2012; Reichwaldt and Ghadouani 2012).
Reichwaldt and Ghadouani (2012) emphasize, however, that little research has examined how rainfall intensity and frequency and the length of dry intervals between significant rainfall events affects the prevalence, timing, severity, and toxin production of freshwater HABs. In addition, other weather conditions, such as increased cloud cover or surface winds, can complicate how runoff from precipitation events interact with cyanobacterial growth. Local features such as soil chemistry, geology, groundwater interactions, and land use add more layers of complexity as they interact with heavy precipitation. Figure 2 outlines many of these interactions.
Conceptual diagram that demonstrates how cyanobacterial blooms (CB) can be affected by rainfall and resulting changes in physical, chemical, and biological variables. The diagram is taken from Reichwaldt and Ghadouani (2012).
Citation: Earth Interactions 28, 1; 10.1175/EI-D-23-0008.1
A lack of precipitation can lead to hydrological drought, causing substantial changes in water quality (Fig. 3; Mosley 2015) and water shortages in streams, lakes, and reservoirs (Seneviratne et al. 2021). Lack of precipitation and subsequent water flow results in longer residence times of nutrients in water bodies during drought (Paerl and Paul 2012). This containment of nutrients in a lake or reservoir can be of particular benefit to HABs when a drought is preceded by heavy rainfall and substantial runoff from fertilized fields. Hence, an increased frequency or severity of drought, especially during the summer, is favorable for harmful algal blooms (Lehman et al. 2020). Still, even lakes in close proximity that experience nearly identical climate conditions and weather events can respond differently to drought conditions. For example, in central Texas, Lake Lyndon B. Johnson is directly upstream of Lake Travis, but each was dominated by a different genus of cyanobacteria (Aphanizomenon vs Limnothrix) and had different chemical compositions, resulting in the former lake becoming eutrophic during an extended drought (2010–15) while the latter lake not (Gámez et al. 2019).
Conceptual diagram that demonstrates how water quality can be affected by drought. The diagram is taken from Mosley (2015).
Citation: Earth Interactions 28, 1; 10.1175/EI-D-23-0008.1
When drought is accompanied by hot temperatures, high evaporation rates of surface waters cause accompanying increases in water conductivity and salinity. Salinization can cause shifts in phytoplankton species because many eukaryotic species cannot tolerate higher salinity; some species of cyanobacteria, however, can live in these changed conditions and may even increase their toxin production (Paerl and Huisman 2009; Paerl and Otten 2013). High salinity levels preceded toxic golden algae (Prymnesium parvum) blooms in reservoirs in the Colorado and Brazos basins of Texas (Patiño et al. 2014). Roelke et al. (2012) found that salinity levels had to reach a threshold before golden algae populations would increase substantially; this threshold may not be reached during a single dry year but require a series of dry years (Fig. 4). In addition, a study of three large reservoirs on the Brazos River (Texas) suggested that if flows were reduced to 40% of their historical levels, then extended inflow events (i.e., longer than 20 days) would decrease from 40 to 1 per decade (Roelke et al. 2012). These inflow events are critical to lake flushing and reducing the risk of Prymnesium parvum (golden algae) blooms.
Conceptual drawing of the relationship between salinity levels (straight red lines), water inflows (blue lines in upper half), and Prymnesium parvum (golden algae) population for reservoirs (represented by the color-shaded areas) in the Brazos basin of Texas. Note that salinity values may need to increase over (b) several dry years after (a) a wet year before (c) they exceed the salinity threshold for an algal bloom to occur. The diagram is taken from Roelke et al. (2012).
Citation: Earth Interactions 28, 1; 10.1175/EI-D-23-0008.1
In humid climates where more annual rainfall is projected for the future, frequent rainfall events may cause sufficient mixing to reduce or maintain the future occurrences of HABs, even with warmer temperatures (Bouvy et al. 2003; Reichwaldt and Ghadouani 2012). In semiarid or arid climates where annual rainfall is expected to be equal to or less than historical conditions, heavier but less frequent rainfall events in the future likely will favor more frequent or severe HABs (Paerl and Huisman 2009; Trainer et al. 2020). Loecke et al. (2017) examined drought-to-flood transitions (also called “whiplash” events) in the Midwest that were characterized by large precipitation deficits (i.e., dry conditions) from July to December followed by precipitation surpluses (i.e., wet conditions) from January to June. They found that the highest spring nitrate concentrations near the mouth of the Iowa River (in a primarily agricultural watershed) occurred in years with drought-to-flood transitions, likely resulting from the springtime precipitation flushing of reactive nitrogen stored in agricultural soils during the prior drought conditions. Using downscaled precipitation projections from 30 global climate models, the authors found that 19 projected an increase and 11 projected no trend in these whiplash events out to 2100. Research on the relationship between drought-to-flood transitions and HABs is needed to determine if the higher nitrate concentrations also result in more frequent or severe blooms.
3. Threats of and monitoring of harmful algal blooms
There are at least 95 known species of cyanobacteria that produce toxins (i.e., cyanotoxins) out of over 2000 species (Wolfe 2021). These toxins include anatoxins, cylindrospermopsins, microcystins, nodularins, and saxitoxins, among many other toxins that are less studied or understood (Loftin et al. 2016). Microcystin- and cylindrospermopsin-producing species are among the most widespread cyanobacteria worldwide (Buratti et al. 2017) and most frequently detected species in freshwater (Campos and Vasconcelos 2010). Microcystin is a potent hepatotoxin (i.e., toxic to the liver; Campos and Vasconcelos 2010), and cylindrospermopsin is both a hepatotoxin and a cytotoxin that targets other organs (Kinnear 2010; Loftin et al. 2016; Pichardo et al. 2017). Microcystins are the most detected cyanotoxin in U.S. lakes and reservoirs (EPA 2009, 2022), yet research indicates that cylindrospermopsins are expanding into temperate zones, exposing more animals and increasing concerns for human and ecosystem health (Kinnear 2010).
a. Threats to companion animals, livestock, and wildlife
Companion animals, livestock, and wildlife can be exposed to cyanotoxins in HABs more readily than humans due to their behaviors and habitats (Backer and Miller 2016). Routes of exposure to cyanobacteria poisoning can be by ingestion, inhalation, dermal contact, or bioaccumulation (Ettoumi et al. 2011). Dogs are particularly vulnerable because they are prone to swim in water bodies regardless of appearance or smell of the water. When they lick their fur, any cyanotoxin clinging to their fur is ingested (Backer et al. 2013). Cattle, sheep, and other livestock are also at risk. For example, from 19 to 23 June 2017, 32 steers died after drinking toxic waters during a cyanobacterial bloom at Junipers Reservoir in Oregon (Dreher et al. 2019). In a similar mass mortality event, nine cows died in Montana after drinking lake water during a bloom (Backer et al. 2015). The full scope of adverse impacts of cyanotoxin poisoning to animals is unknown and often misdiagnosed (Backer et al. 2013).
Using reconstructions of environmental conditions from sediments, it is clear that cyanotoxins have been present in some water bodies since at least the 1800s (Zastepa et al. 2017). Australian Aboriginal people have been aware of cyanobacteria poisonings in Lake Alexandrina in South Australia since 1850 (Stewart et al. 2008). Any animal, from large to small, can be adversely affected by cyanobacteria poisoning. For example, in June 2020, news media reported the sudden deaths of over 330 African savanna elephants (Loxodonta Africana) in southern Botswana, presumably from biotoxins produced by cyanobacteria (Wang et al. 2021).
A mysterious mass killing of bald eagles (Haliaeetus leucocephalus) and other avian species in the southeastern United States took close to 30 years and the collaboration of researchers from multiple disciplines to solve (Breinlinger et al. 2021). Between 1994 and 1996, more than 70 bald eagles died at DeGray Lake in Arkansas (Thomas et al. 1998). According to Breinlinger et al. (2021), investigators found that the birds suffered from neurological impairment and proposed that a neurotoxin was to blame. The lake had invasive aquatic vegetation, Hydrilla verticillata, with the cyanobacterium Aetokthonos hydrillicola, which the researchers hypothesized produced the toxin. When they failed to produce the neurotoxin in the laboratory setting, they searched for another factor. They discovered that a bromine compound (e.g., from power plants, fungicides, or gasoline additives) covered the leaves of the invasive plant and was needed by the cyanobacterium to produce the toxin, finally solving the mystery.
Cyanotoxin poisoning is not limited to large fauna. Stewart et al. (2008) described the mortality of 84 honeybee hives in in 1971 in New South Wales, Australia, that was attributed to the cyanobacteria, Anabaena circinalis. In 1985, over 1000 animals died, including more than 500 bats and 24 mallards, on a lake in Alberta, Canada, with a cyanobacteria bloom that produced the neurotoxin anatoxin-a. In 1952, a large cyanobacteria bloom on Storm Lake, Iowa, included Anabaena flos-aquae, a neurotoxin, killed thousands of gulls, ducks, coots, pheasants, and songbirds, as well as many small mammals of wildlife and companion animals.
b. Threats to human health
Humans typically are exposed to cyanotoxins through oral or dermal exposure (Fig. 5) to contaminated water (Hilborn and Beasley 2015). Recreational activities that aerosolize microcystins, such as jet skiing, water skiing, and boating, can increase the risk of exposure and respiratory illnesses (Cheng et al. 2007). Wind can drive some buoyant species’ cells to accumulate along impediments and shorelines, and wind turbulence can disrupt clusters of cells or colonies both vertically and horizontally, providing additional routes of exposure to people recreating in water (Backer et al. 2010). Water recreation increases during the warm season, increasing the chance for exposure to HABs in inland waters (Brooks et al. 2017). Although cases of human illness from HABs have been documented worldwide, a review by (Svirčev et al. 2017) of published epidemiology papers found only minimal documentation of human morbidity and mortality from cyanobacteria poisoning. One incident occurred in Brazil in 1996 when dialysis patients accidently received contaminated water intravenously during the dialysis procedure, resulting in 100 patients with acute liver failure and 76 deaths (Hilborn and Beasley 2015; Svirčev et al. 2017). In 2011, the Kansas Department of Health and Environment received 25 reports of human illnesses that were potentially associated with freshwater HABs; 13 cases were classified as suspect and 7 were confirmed to result from freshwater HAB exposure (Trevino-Garrison et al. 2015). In a well-publicized event, U.S. Senator J. Inhofe became gravely ill after swimming through a Microcysitis bloom at his vacation home on Grand Lake (Oklahoma) in 2011 (Berg 2011).
Child playing in harmful algal bloom at Lake Byllesby Reservoir in the Cannon River Watershed of Minnesota. Credit: Minnesota Pollution Control Agency (2003).
Citation: Earth Interactions 28, 1; 10.1175/EI-D-23-0008.1
Numerical criteria have been developed for cyanotoxins, primarily focusing on human health risks from recreational exposure. For example, a 2019 document from the EPA provides recommendations for states and tribes on the criteria and policies for monitoring and responding to HABs with microcystin or cylindrospermopsin toxins (EPA 2019). The EPA recommends issuing a swimming advisory based on exceeding 8 μg L−1 for microcystin or 15 μg L−1 for cylindrospermopsin for any single day. Similarly, the World Health Organization (WHO) has published risk-level guidelines for recreational exposure to cyanobacteria based on the severity of acute health effects to humans (WHO 2003). WHO risk levels (low, medium, and high) are based on the concentration of cyanobacteria (in cells per milliliter), with corresponding levels of microcystin (in micrograms per liter) estimated and probable acute health effects on humans (Table 1).
Risk levels for recreational exposure to cyanobacteria as established by the World Health Organization (WHO 2003).
c. Monitoring harmful algal blooms
The EPA was created in 1970 to protect the land, water, and air of the United States. One of the first major environmental laws under the purview of the EPA was the Clean Water Act of 1972. The intent of the Clean Water Act is to ensure that the nation’s water quality is at a level that is safe for human health and aquatic life. The EPA gave states and, through later amendments to the Clean Water Act, tribes, with authority over most environmental laws. It is the state or tribe that develops water quality standards for the purpose of maintaining water quality in the water bodies for which they have jurisdiction (EPA 2014).
Approaches to monitor the occurrence and toxin quota of harmful algal blooms in freshwater systems vary across states, tribes, and federal agencies. Governments are challenged with the expense of routine monitoring, which not only can include sample collection but also laboratory analysis. Microscopic identification and cell counting are basic techniques for monitoring cyanobacterial blooms but still require the expertise of microbiologists (Srivastava et al. 2013). Some states include routine monitoring during the outdoor recreational season, when swimmers, fishers, and boaters may be most affected. Nebraska conducts routine monitoring through its Nebraska Beach Watch program (Nebraska Department of Environment and Energy 2022), details of which can be found in Walker et al. (2008). Other states, such as Kansas, have written response procedures to HABs that include methods to collect samples, criteria for advisories, and procedures to respond to complaints or notify citizens of potential HABs (Kansas Department of Health and Environment 2020). Oklahoma’s Department of Tourism notifies the public of lake conditions on their website, including when a water body meets the WHO guideline (Table 1) for moderate probability of adverse health effects (TravelOK 2022). The EPA provides a comprehensive list of states that monitor HABs on its website (https://www.epa.gov/cyanohabs/state-habs-monitoring-programs-and-resources).
For tribes, water is sacred and life giving. It often is an integral component in many tribes’ ceremonial practices (Cozzetto et al. 2014). Thus, tribes approach HAB monitoring from the perspective of protecting or restoring that sacredness rather than a simply utilitarian approach. For example, the Yurok people have had an intricate relationship with the Klamath River. The river is part of their creation story and used in most of their ceremonies (Tanana 2022). However, climate-driven impacts and point and nonpoint source pollutants have affected tribal traditions for the Yurok Tribe of California. Because of the increase in HABs, dams, and pollutants that adversely affected salmon and water quality, the Yurok Tribe passed a resolution in 2019 that gives personhood to the Klamath River (Cordtz 2020).
There also are tribes across the United States, primarily in the West and Northwest, that have active freshwater monitoring programs, and several tribes are in monitoring consortiums. For example, the Klamath Basin Monitoring Program (KBMP) is an interstate, intertribal, and multiagency program that coordinates and collaborates on water-quality monitoring throughout the Klamath Basin of California and Oregon (KBMP 2022). Program members monitor for potential toxigenic cyanobacteria from May through November by collecting offshore grab samples for laboratory analysis (KBMP 2022). Another robust HABs-monitoring program is coordinated by the Big Valley Band of Pomo Indians and the Elem Indian Colony, who have monitored HABs on Clear Lake in California. In 2014, these two tribes collaborated to start a monitoring program with eight sites on the lake; now they monitor 20 sites, including conducting microscopy to determine genera and collecting fish and shellfish to analyze tissue for presence of cyanotoxins (Big Valley Rancheria 2022).
The Harmful Algal Bloom and Hypoxia Research and Control Act of 1998 (and later amended) established a federal interagency working group to guide research, monitoring, and forecasting efforts for HABs and hypoxia in fresh, estuarine, and marine waters of the United States. In a 2022 report, the U.S. Government Accountability Office (GAO 2022) recommended that this working group should develop a framework for expanding monitoring and forecasting freshwater HABs, including identifying the resources needed and prioritizing the water bodies for these efforts. Federal agencies such as the EPA, National Aeronautics Space Administration (NASA), NOAA, and the U.S. Geological Survey (USGS) also are partnering with tribes, states, and other local agencies through the Cyanobacteria Assessment Network to monitor and respond to freshwater HABs (GAO 2022). The network is working on the following objectives: 1) to develop a systematic approach to identify cyanobacteria blooms across the contiguous United States using oceanic satellites, 2) to characterize exposure and human health effects in recreational and drinking water sources, and 3) to characterize responses and the economic value of a HABs early warning system.
In addition to collecting and analyzing water samples, monitoring of freshwater HABs has expanded with new tools and technologies, from simple to complex and from inexpensive to costly. Continuous, in situ monitoring can be conducted using sensing probes that are attached to permanent monitoring stations, such as buoys, as changes in water quality can indicate a cyanobacteria bloom (Grand River Dam Authority 2021). Sensors include those that measure water-quality variables and those that measure the fluorescence of chlorophyll-a and phycocyanin pigments. One simple and inexpensive method of detection of a potential harmful algal bloom is visual inspection by citizens and pilots in programs like those from the U.S. Office of Harmful Algal Blooms and NASA’s Glenn Research Center (Ansari and Schubert 2018). Washington state agencies worked with lake residents (Hardy et al. 2016) and citizen science groups such as CyanoTracker (Scott et al. 2016) to teach them how to recognize potential HABs and CyanoHABs. After a potential HAB is reported, government agencies can confirm through water sampling and analysis. Repeated, uniform water sampling and analysis for a large region can be expensive, however, so most states do not invest in these programs (Clark et al. 2017). For example, monthly monitoring of 100 lakes in Oklahoma was estimated to cost $3.5 million (in 2012 U.S. dollars) annually (Smithee et al. 2012).
Satellite remote sensing has also been used to measure the size and duration of cyanobacteria blooms, using algal pigments as proxies for HAB abundance (Clark et al. 2017). Coffer et al. (2020) used satellite data to detect and report the weekly percentage of lakes across the contiguous United States that experienced cyanobacterial blooms. This type of information can be applied to prioritize where more expensive, in situ monitoring is needed. Ignatius et al. (2022) examined 60 reservoirs in the south-central United Sates over five years using the Ocean and Land Color Instrument of the European Space Agency (ESA) to determine whether there were within-reservoir spatial or temporal trends in HABs. These types of measurements also can aid reservoir managers in scheduling in situ monitoring and preparing materials for seasonal health alerts. Using the same ESA product in real time, Schaeffer et al. (2018) created a graphical display application for smartphones that managers can use for low-cost, rapid assessments of water quality. Limitations remain, however, in satellite measurements: they have relatively coarse resolution, only detect near-surface conditions, use algorithms that can introduce biases or errors greater than those from direct sampling, and clouds, aerosols, or other spectral interference can obscure the bloom (Clark et al. 2017; Wu et al. 2019).
Other monitoring methods apply passive remote sensing technologies from uncrewed aerial systems (UAS). UASs have been equipped with sensors (Fig. 6) to measure bloom occurrence, extent, and density through a variety of spectral bands (Wu et al. 2019), but they also have been employed to collect and analyze water samples directly (e.g., Koparan et al. 2018). Although current limitations on battery power, sensor-package weight, wind turbulence, and flying restrictions have curtailed the use of UAS for monitoring HABS, future changes in technologies and policies are expected to open new opportunities for UAS-based monitoring (e.g., Koparan et al. 2018). Recent uses of light detection and ranging (lidar) for active remote sensing also have promise, especially because of the lidar’s ability to optically detect biochemical information beyond the air–water interface (Moore et al. 2019; Zhao et al. 2023). Signal attenuation, errors resulting from algorithm development, and high instrument cost limit the usefulness of lidar for regular monitoring at this time.
A UAS surveys the York River in Virginia to study harmful algal blooms (Dong et al. 2011). The photograph was provided through the courtesy of D. Gong, Virginia Institute of Marine Science.
Citation: Earth Interactions 28, 1; 10.1175/EI-D-23-0008.1
4. Discussion and summary
Climate change stressors, such as warmer air temperature, lengthening warm seasons, increased intensity of heavy rainfall events, and longer or more severe droughts, have been linked to an increase in the frequency and severity of harmful algal bloom occurrences in freshwater systems. The number of severe lake heatwaves has increased sixfold between 1995–2004 and 2010–19 (Woolway et al. 2022), increasing the risk of HABs in locations where temperatures remain in the optimal range for cyanobacteria growth. The rate of eutrophication in many temperate lakes has increased, primarily from increasing anthropogenic nutrient inputs and more runoff during heavy rain events (e.g., Bennett et al. 2001), so nutrient levels usually are high enough for HAB development and sustenance. A combination of eutrophication and warmer water temperatures contributes to increasing lake stratification, favoring the growth of certain cyanobacteria species and the proliferation of phytoplankton overall. Blooms tend to be modulated by weather and climate variables (Zhang et al. 2012) but other factors typically are associated with changes in HAB prevalence, timing, and toxin production (Griffith and Gobler 2020).
Although it is difficult to isolate specific effects of climate change on cyanobacteria growth, it is evident that climate change impacts, such as warmer temperatures, heavier rainfall events, and extended warm seasons, favor conditions for cyanobacteria growth (Behrenfeld et al. 2006; Heisler et al. 2008). In addition, changes in wind speed (i.e., affecting surface turbulence) and solar radiation (i.e., affecting photosynthesis) with climate change can be locally variable (Glibert 2020; Wells et al. 2020), leading to complexities in their effect on HABs (Jöhnk et al. 2008).
Across much of the United States, air temperatures are projected to increase, heatwaves are expected to increase in frequency and length, and growing seasons are projected to lengthen. Across the semiarid and arid regions of the United States, drought frequency and severity are projected to increase from increased evaporation or decreases in precipitation. Also, heavy-rain events that tend to flush surface waters or cause surface-layer mixing in lakes are expected to become more frequent. Future changes in cloud cover and surface winds are uncertain. Based on studies conducted across freshwater systems in the contiguous United States, these projected changes portend an increase in the frequency and severity of harmful algal blooms, including the potential for novel locations for HAB occurrence, novel strains of cyanobacteria, and higher toxin production of blooms. The paucity of HAB research in many freshwater inland water bodies precludes more specific forecasting of future changes.
The increase in the frequency and severity of HABs challenges resource managers and users to monitor for toxic blooms and publicly report them and their associated public health alerts. These blooms can cause sickness, and even death, in humans, companion animals, livestock, and wildlife. Species that previously have not been exposed to a specific HAB-produced toxin likely are at higher risk (Jöhnk et al. 2008), so monitoring is important even in water bodies where a HAB would be novel. Yet, the monitoring policies and HAB management approaches vary widely among federal agencies, states, tribes, and local governments. Some states have increased their monitoring efforts, which may account for measured increases in HAB occurrences and complicate the detection of a climate change (or other) signal.
Detection of HAB-related illness in humans is challenging because there currently are no diagnostic tools that test specifically for HAB-related toxins; diagnosis often is determined by the exclusion of other potential causes (Harris et al. 2020). Yet animals, especially canines, can be used as sentinels to recognize HAB-related illness in humans because these animals are more likely to interact directly with the toxic blooms (Backer and Miller 2016). Even within a state, however, professionals from different health and environmental departments may not be communicating with one another about HABs, leading to siloing of information and insular actions for preparation and response.
As a result, surveillance of and response to HABs can benefit from a “One Health” approach. The One Health concept recognizes the connection of health risks and outcomes among humans, companion animals, livestock, wildlife, and the environment they inhabit (Hilborn and Beasley 2015). It is a holistic, collaborative, multisectoral, and transdisciplinary approach that already has been proven successful over thousands of years through traditional knowledge, Native science, and Indigenous worldviews (Hueffer et al. 2019; Jack et al. 2020). In 2014, the Centers for Disease Control and Prevention (CDC) expanded their One Health initiatives to address the increase of HABs and the reporting of HAB-related illnesses in humans and animals through the One Health Harmful Algal Blooms System (OHHABS). With training and surveillance tools provided by OHHABS, the New York State Department of Health piloted a program the following year for an illness surveillance system in 16 counties. The program focused on communication about and reporting of HABs from the public, local public health departments, veterinarians, and physicians (Hueffer et al. 2019). The pilot project resulted in an increase in the verified cases of HAB-related illnesses in both humans and dogs. Prior to the pilot, the New York State Department of Health had not exceeded 10 reported cases that met the CDC criteria; during the program, there were 35 cases of HAB-related illnesses in humans and three in dogs. As a result of the successful pilot, the CDC officially launched OHHABS in 2016 (Roberts 2020) as a nationwide voluntary reporting system. Between 2016 and 2018, 18 states voluntarily reported 421 HAB events (Roberts 2020).
There is a need for additional research on, monitoring of, and education about HABs across inland regions where future climate conditions are likely to increase the frequency of these events. Better understanding of the interactions among climate change, land-use practices, and other anthropogenic drivers of HAB formation and development will provide the science community a better opportunity to develop successful mitigation or adaptation methods. Programs to monitor HABs can be developed across multiple sectors, as in the One Health approach, so that experts can learn from one another. Education programs, especially through those who are trusted in local communities (e.g., medical professionals, park managers, public safety officials), can better prepare communities for future blooms. Until climate warming is mitigated through substantial actions to reduce and remove anthropogenic greenhouse gases in the atmosphere, harmful algal blooms appear to be an increasing threat to health that needs to be addressed aggressively.
Acknowledgments.
This work was supported by the South Central Climate Adaptation Science Center at the University of Oklahoma with funding from Grants 10553130 and 20003905 from the U.S. Geological Survey. We are grateful for the internal review of and feedback from Dr. Sharon Hausam.
Data availability statement.
No datasets were generated or analyzed during the current study.
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