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Harmful algal blooms (HABs) have been observed in nature for centuries, but recently these blooms have increased in frequency and intensity in both fresh and marine waters (O’Neil, 2012). Many studies have shown that eutrophication of water bodies, increased water temperature, more intense precipitation, and introduction of invasive species have played a significant role in the escalation of HABs (Vanderploeg, 2001), (O’Neil, 2012), (Paerl & Otten, 2012). The New York Department of Environmental Conservation (DEC) notes that HABs in freshwater lakes in Central New York are typically dominated by cyanobacteria, and microcystin is the most frequently detected cyanotoxin (DEC, 2018). Skaneateles Lake, the primary drinking water source for the City of Syracuse, has experienced several HABs over the last few years with confirmed toxin production. As high as 723μg/L of the toxin microcystin was detected in the lake in August of 2018, and acutely toxic effects are highly probably at concentrations between 20 – 2,000 μg/L (Skaneateles Lake Association, 2018), (EPA, 2019). These blooms have presented engineering challenges for drinking water plants that use HAB-plagued lakes as water sources. Actions such as reduction of nutrient pollution to the lake and reduction of invasive species should be considered to reduce the frequency of HABs.
Algae make up a diverse group of photosynthetic organisms that are essential to sustain life on earth because of their functional roles as an energy base in the food web, as well as their contributions to earth’s biogeochemical cycles. That being said, most algae are harmless, but when environmental conditions are favorable it can cause them to grow out of control and negatively impact their surrounding environment. Algae thrive under high nutrient, high temperature, calm water conditions, and often become a problem when there is an excess amount of nutrients flowing into a water body (O’Neil, 2012). As seen in Figure 1 when this process occurs, these microscopic algae can physically take over a body of water, resulting in severe adverse impacts to the aquatic ecosystem. Some microalgae can produce harmful toxins resulting in what is known as a Harmful Algal Bloom (HAB). During the bloom – the algae can block other photosynthetic organisms from getting access to light. In addition, when the blooms eventually senesce, it results in oxygen depletion of the water body from the aerobic decomposition of the dead algae by other microorganisms.
HABs are a natural phenomenon, however in recent years they have become far more frequent and intense than in the past (O’Neil, 2012). There are many factors that contribute to the increase in HABs, and some major factors include eutrophication of water bodies, increasing water temperatures, and introduction of invasive species (Vanderploeg, 2001) (O’Neil, 2012) (Paerl & Otten, 2012). Anthropogenic nutrient pollution leads to the eutrophication of lakes, and is a major challenge to manage because it can be difficult to pinpoint and control sources of nutrients into the water bodies. Nutrient pollution can come from a variety of human related activities such as agricultural fertilizers, animal manure, wastewater treatment plant (WWTP) effluent, storm water runoff, and failing septic tanks (DEC, 2018). Nitrogen and phosphorus are the main nutrients of concern in regard to HABs. A study in New York State showed that for every 0.01 mg/L increase in total phosphorus levels, the probability that a lake in New York will have a HAB in a given year increases by about 10% to 18% (DEC, 2018).
HABs have been known to develop over a wide range of water bodies from oceans to lakes and ponds. Nationwide, toxic HABs have been implicated in human and animal illness and death in at least 43 states. In August 2016, at least 19 states had public health advisories because of CyanoHABs (EPA, 2019). HABs may occur anywhere along the nation’s coast or lakes, especially during the summer. Red tide events caused by blooms of the harmful algae Karenia brevis are particularly common in coastal regions of Florida and Texas (National Ocean Service, 2019). An unusually persistent HAB (red tide) affected portions of the coasts of Florida between 2017-2018, dissipating in the winter of 2018/2019. It persisted on the southwest coast beginning in October 2017 and spread to the Panhandle and the east coast of Florida. A short-lived bloom also occurred in Texas in September 2018. Red tides, caused by Karenia brevis algae, produce toxins that can cause fish kills, respiratory irritation, and mortality of sea turtles, manatees, birds, and dolphins (National Ocean Service, 2018). While red tide caused by dinoflagellates such as Karenia brevis are the leading cause of HABs in oceanic waters, cyanobacterial-dominated HABs (otherwise known as blue green algae) are the variety of HABs dominating freshwater lakes and reservoirs all over New York State (DEC, 2018).
Figure . The outline shows the watershed area of Skaneateles Lake. All rain, snow, and stream, and storm water runoff eventually flow into the lake CITATION NYD18 \l 1033 (DEC, 2018).
The DEC has reported several hundred confirmed cases of CyanoHABS in water bodies in New York since 2012 reported (DEC, 2018). Major freshwater sources such as Lake Erie, Owasco lake, and Skaneateles lake have all been plagued with HABs. Skaneateles Lake, a seen in Figure 2, is an 8,704-acre lake in central New York that is the fifth largest of the Finger Lakes, is one of the State’s 12 identified “priority lakes” in regard to vulnerability to HABs (DEC, 2018). These priority lakes are being studied to identify what factors are causing the HABs and what actions can be taken to reduce blooms. The lake is used for swimming, fishing, boating, and other water recreation. In addition, Skaneateles Lake is the primary drinking water source for the City of Syracuse, and also provides drinking water to portions of the towns of DeWitt, Onondaga, Geddes, Camillus, Salina, and Skaneateles, and to the Villages of Skaneateles, Jordan, and Elbridge (City of Syracuse, 2018).
Dozens of news articles have been released regarding HABs in Skaneateles Lake, stirring up questions and fears about algae toxins passing through the City of Syracuse drinking water treatment plant and on to consumers. For example, as seen in Figure 3, on September 20th, 2017 Syracuse.com had a headline article “Algae toxins in Syracuse water system: What we know so far (and what we don’t).” This article discussed how toxins were detected in drinking water from the lake in the town of Skaneateles. It mentions that the concentration was below the EPA’s 10-day health advisory level of 0.30 μg/L for sensitive populations, and was safe for residents to drink, but also indicated that the city should consider investment of a carbon filtration system to provide absolute protection from toxins (Coin, 2017). These kinds of articles can lead to public distrust in the city and their water supply, but they also call governing agencies into action to study the issue and find proactive solutions. In the lake itself, concentrations as high as 723 μg/L of microcystin were detected in August of 2018, however levels this high have not been detected in the drinking water (Skaneateles Lake Association, 2018). Acutely toxic effects are highly probably at concentrations between 20 – 2,000 μg/L. Chronic effects at low concentrations are not as well understood, but the EPA 10-day drinking water health advisory of 0.3 μg/L is considered a conservative number for sensitive populations (EPA, 2019). Additional advisory levels are listed in Table 1 for various cyanotoxins and effected populations.
Figure . Headline from Syracuse.com during the September 2017 HAB outbreak on Skaneateles Lake, NY CITATION Coi17 \l 1033 (Coin, 2017).
The DEC’s report on Skaneateles HABs indicated that nutrient loading to the lake is primarily from nonpoint sources, 80% of which is attributable to agricultural land (DEC, 2018). In response, New York State is implementing new regulations and action plans to tackle this growing issue. The actions include regulations on topics such as runoff reduction, best management practices on croplands and non-agricultural lands, roadside ditch projects, and riparian habitat stabilization. A strong focus in the regulations is being placed on reducing the occurrence of HABs rather than investment in advanced water treatment technologies, where they can be avoided (DEC, 2018).
The growing problem of HABs in central New York can be better understood when observed through the lens of the fundamentals of environmental microbiology.
Fundamental Environmental microbiological principles
There are many fundamental microbiological concepts to consider when trying to understand and search for methods to minimize the occurrence and intensity of HABs including the exponential growth curve, biogeochemical cycles, microbial energetics, growth rates, and nucleic acid based methods of analysis.
Exponential growth is when a population grows at a rapid rate, relatively unchecked by competition. It eventually reaches equilibrium where the number of organisms dying matches the number being produced. As seen in Figure 4, eventually, this process results in the “death” phase, where the microorganism has exhausted all of a certain resource resulting in the death of most of the population. It is important to understand that the exponential growth phase of HABs do not directly cause the oxygen depletion of water, given that they are photosynthetic microorganisms. Oxygen is the preferred electron acceptor for degradation of organic material by heterotrophs, as it provides the greatest redox potential when paired with any electron donor (Costello Staniec, 2019). Once the HAB reaches the death phase of the growth curve, the cyanobacteria lyse their organic material into the water. Then, heterotrophic microorganisms in the lake then use up oxygen to decompose the now abundant organic matter, which results in the oxygen-depletion of the water body. The eventual senescence of freshwater HABs is typically thought to be a result of phosphorus depletion, though this is not the cause in every case (Paerl & Otten, 2012).
It is atypical to see exponential growth of microorganisms in the environment as there typically is competition over resources, resulting in a limited growth of any particular population. Most cyanobacteria are obligate photoautotrophs, using sunlight in the photic zone of the marine environment as their energy source, and fix inorganic carbon (carbon dioxide or bicarbonate) for their carbon source (Madigan, 2009, p. 41). There are a few cyanobacterial species that can assimilate inorganic nitrogen from the atmosphere, but generally speaking they require these nutrients to be available their aquatic environment to build important macromolecules and carry out cell functions (Madigan, 2009, p. 466). For this reason, typically in the natural environment nitrogen and phosphorus would limit the exponential growth of these types of microorganisms, but in eutrophic lakes – with high nutrient concentrations – cyanobacteria can grow exponentially. Eutrophic lakes can occur naturally based on the geology and nutrient cycles of a particular lake, but human activities have been creating more eutrophic water bodies through nutrient pollution (EPA, 2019). Many studies have shown that lakes impacted by anthropogenic nutrient pollution provide more favorable conditions for exponential growth of cyanobacteria (Woodhouse, 2016), (O’Neil, 2012), (Paerl & Otten, 2012).
As seen in Figure 5 there are many conditions in addition to nutrient overload that can impact the growth rate observed during the exponential phase of the growth curve (Paerl & Otten, 2012). Low nitrogen to phosphorus ratios, long water residence time, high dissolved organic matter, water temperature, grazing rates of algae predators, and light levels all can result in increased HAB frequency by promoting their exponential growth. One of these factor that shows why CyanoHABs in particular may be on the rise is the temperature impact on cyanobacteria growth rates. Figure 6 shows that the maximum growth rate of common cyanobacteria species occurs in warmer waters, generally above 25℃ (Paerl & Otten, 2012). Given that climate change is resulting overall average higher temperatures – it makes sense that CyanoHABs are on the rise since the environment is becoming more ideal for their rapid growth (Woodhouse, 2016). In addition, climate change has resulted in less frequent but more intense rainfall, which tends to increase the amount of nutrient runoff into water bodies (Chen, Hu, & Guo, 2015). As discussed above this contributes further to eutrophication of water bodies and promotion of exponential growth of algae. Understanding the principles of exponential growth of HABs can help engineers and scientists to figure out what conditions may lead to blooms, and what they can do to mitigate them.
Figure . There is a wide range of both positive and negative effectors and modulating environmental conditions that can influence the intensity and frequency of CyanoHABs CITATION Pae12 \l 1033 (Paerl & Otten, 2012).
Another fundamental topic of microbiology that is important to collecting information on HABs is nucleic acid-based methods of analysis. These methods are particularly important when considering toxin-production during HABs. As discussed above, not all algal blooms result in toxin production, and little is understood as to what causes the cyanobacteria to turn on the gene to produce toxins. Researchers have identified that certain gene clusters result in the production of toxins for a variety of species of HABs, and are trying to figure out what conditions turns these genes on and off (Brunson, McKinnie, Chekan, McCrow, & Miles, 2010). Finding the genes that result in toxin production activation in cyanobacteria could provide engineers and scientists with important details on what can be done to reduce the occurrences of CyanoHABs. Polymerase chain reactions (PCR) has been used for identifying, enumerating, and studying the genetic makeup of toxic algal species in aquatic ecosystems (Antonella & Luca, 2013). The cyanobacteria gene clusters responsible for the synthesis of microsystins, nodularin, and cylindrospermopsin have been identified, and quantitative PCR method can be used to study these blooms. However, the method needs to be optimized to the local cyanobacteria population in the area under investigation due to variations in target genes across microbial strains, and to make sure the primer works with the environmental sample to get accurate results (Pacheco, Guedes, & Azevedo, 2016). PCR is a powerful tool in the pursuit to understand HABs, and could eventually provide better ability to predict when blooms will occur and how they could be prevented.
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In addition, PCR could provide water treatment plants with information sooner than conventional analytical tests for algae toxins (Pacheco, Guedes, & Azevedo, 2016). This information will help them when deciding whether or not to shut off certain intakes, or to turn on optional treatment trains that can remove algae toxins. Depending on the technologies used at water treatment plants, algae toxins may or may not get removed in treatment. The Skaneateles Lake water treatment plant does not have any form of filtration (which typically is mandatory for surface waters) because it has a filtration waiver (City of Syracuse, 2018). This waiver saves the City of Syracuse in operating costs for the treatment plant, but it also leaves the system at greater risk during HAB events as there is no way to filter out the algae. As discussed above, in recent years, algae toxins have been detected in the influent to the water treatment plant in Skaneateles. Despite the fact that the treatment plant has emergency storage for (4) days’ worth of water, the plant didn’t realize fast enough that a toxic bloom was occurring, and so they brought contaminated water into the system (Coin, 2017). PCR and other nucleic acid based methods of analysis may provide water treatment plant operators with faster information about whether a bloom contains harmful toxins, letting them know they need to shut off their intakes.
By understanding these fundamental principles of microbiology, engineers and scientists can develop effective solutions to the rising challenge of HABs.
Engineering challenges of habs
There are many aspects of HABs that create engineering challenges. They can bloom rapidly in a large scale, and in a pattern that is very hard to predict. Everything in the watershed of the lake could have an impact on blooms, and this presents engineering challenges due to the substantial efforts required of any solution, and associated costs. Some lakes have very large watershed areas, and so it can be overwhelming to try to address all the potential factors that contribute to blooms. Algal blooms do not always produce toxins, and as mentioned above, it takes time to confirm if the bloom is producing toxins. Despite the challenges, actions need to be taken by scientists to mitigate the great expansion of HABs to protect both people and the environment. Currently, many water treatment plants are reliant on management practices that just cover up the effects of HABs, rather than prevent them. For example, a common method employed to protect human health from algae toxins in drinking water is by using deeper water treatment intake pipes. Algae blooms generally occur near the surface since they are photosynthetic organisms, and so if the water treatment plant can draw from a deeper water intake during blooms, they may be able to minimize uptake of algae and toxins (City of Syracuse, 2018). However, not all lakes are deep enough to avoid algae entirely. Lakes plagued by HABs that are drinking water sources are starting to add treatment steps to remove toxins, such as adsorption by activated carbon. In addition, chlorine can be used to neutralize the toxin, but at the risk of producing disinfection byproducts (DPBs) (EPA, 2018). Table 2 shows the relative effectiveness of disinfection chemicals in oxidizing various cyanotoxins. These engineering solutions, however, do not help to prevent HABs, they just address the immediate threats to human health after a bloom occurs.
In order to reduce the frequency and intensity of HABs, anthropogenic nutrient pollution needs to be managed better. As discussed above, Skaneateles Lake predominantly receives nutrients from non-point source pollution, predominately from agricultural runoff (DEC, 2018). There are many proposed methods for controlling the influx of nutrients to water bodies including runoff reduction, best management practices (BMPs) on croplands and non-agricultural lands, roadside ditch projects, and riparian habitat stabilization (DEC, 2018). A specific example of a method to reduce runoff is through the development of riparian buffers. These are areas near the shore of waterbodies where trees, shrubs, and grassed can be planted to capture nutrient-laden sediments before they reach the waterbody (DEC, 2019).
BMP practices for agricultural fields could include alternative planting strategies such as conservation tillage (also known as “no till”). Conservation tillage, as shown in Figure 7, not only prevents runoff of sediments, it also can improve the infiltration of water into the soils and make for better agricultural productivity, with less nutrients needed to be supplemented (DEC, 2019) (Carter, 2005). There are four main types of conservation tillage which include mulch tillage, ridge tillage, zone tillage, and no-tillage (Carter, 2005). No-tillage involved directly injecting seeds into the soil without any mechanical mixing of the soil, and is the most effective at reducing sediment and nutrient runoff. However, it is generally difficult to use in cool, wet soils, such as may be present in Central New York (Carter, 2005). For this reason, it may be more practical to use methods such as mulch tillage in the Skaneateles Lake watershed. Mulch tillage allows for traditional soil mixing for planting and fertilizer application, but leaves at least 30% plant cover on the surface of the plot to help to slow down runoff and reduce the erosion of the sediments and nutrients (Carter, 2005). By reducing soil and nutrient runoff through conservation tillage practices, farmers can not only help to protect Skaneateles Lake from nutrient pollution and subsequent HABs, they also can save money by keeping the nutrients where they want them: in their fields, helping their crops to grow.
As mentioned, invasive species are also highly correlated to the increase in the frequency and intensity of HABs. The infestation of Skaneateles lake with invasive zebra mussels, common carp, Eurasian watermilfoil, quagga mussel, European rudd, and rainbow trout all impact the frequency and duration of HABs (DEC, 2018). Both the common carp and Eupean rudd fish feed on macroinvertebrates that hide in the sediments on the bottom of lakes. These fish stir up the lake sediments in pursuit of their prey, releasing nutrients and sediments into the water column (DEC, 2018). The watermilfoil pulls nutrients from the lake sediments to carry out its biologic processes, but when the plant dies it releases those nutrients that were once trapped in the sediment into the water column. The invasive mussels have been shown to reduce the quantities of cyanobacteria competitors, as they selectively filter feed on the other variety of microorganisms in the lake (Vanderploeg, 2001). This results in increased resource availability to the cyanobacteria, giving them further opportunity to make use of the nutrients available in the lake. It was shown that there is an increased likelihood of annual HABs between 18%-66% for lakes that have invasive mussels present (DEC, 2018).
It can be a major challenge to try to remove invasive species from a water body. In 2012, Skaneateles Lake initiated an Invasive Species Prevention Program to provide recreational users of the lake with guidance on how to prevent the spread of invasive species, as shown in Figure 8. The group has had some success in reduction of watermilfoil, though annual harvest still need to be performed to keep the population at bay (DEC, 2018). It is a much larger challenge to remove the animal variants of invasive, especially the mussels which embed in the sediments. Physical, chemical, and biological methods have been proposed to manage these populations, but there is no “silver bullet” as these methods all have the potential to harm other native species just as much as the invasive targets (Invasive Mussels Collaborative, 2018). For example, Zequanox® is a compound that utilizes a chemical produced by a common soil bacterium, Pseudomonas fluorescens to target zebra and quagga mussels. It destroys the digestive system lining of the mussels, but it cannot be specifically target to just the invasive species (Invasive Mussels Collaborative, 2018). This would potentially destroy native populations unintentionally. However, if after treatment native varieties were reintroduced, it may be worth the temporary disturbance to the ecosystem in the long run. Biological controls could be placed by introducing species that would feed on the invasive mussels, however if a suitable native species is not available then that newly introduced species may become the next problem to manage. Physical treatments could include benthic matts, which are placed on the bottom of the lake. They block oxygen, water, and food from getting to the mussels buried below the benthic matt, eventually starving them out. This, while effective, would also impact any native sediment-dwelling organisms (Invasive Mussels Collaborative, 2018).
If invasive species can be managed by one of the physical, chemical, or biological methods described, it is very critical to educate the public about how invasive species are transported and how to prevent reintroducing them to the lake. Once eradicated, it would be too easy for invasive to be reintroduced to the lake by unaware recreational users of Skaneateles.
One unique and lightly studied method to control HABs is the introduction of genetically modified viruses to interfere with the growth of cyanobacteria. A cyanophage LEP virus has been studied and could prevent the occurrence of CyanoHABs by breaking down the algae structure to disrupt he algae growth and pigment production. Cyanophages are viruses which only destroy their host, cyanobacteria, by adding or deleting genes of cyanobacteria (Ha, 2017).
There are many associated engineering challenges to all of the mitigation strategies discussed above. A combination of these approaches may give the greatest odds to reduce HABs and their impact on the citizens of Central New York and the health of the Skaneateles Lake watershed.
As discussed, HABs, and particularly CyanoHABs, are becoming a serious problem in the United States and in Central New York in particular. Anthropogenic nutrient pollution, climate change, introduction of invasive species, and many other factors have led to an increased frequency and intensity of HABs in freshwater lakes. The toxins produced by these blooms can hurt people and animals, and if present in drinking water could be dangerous to human health. CyanoHABs are the result of favorable environmental conditions for the exponential growth of blue-green algae, and scientists and engineers can use nucleic acid based methods of analysis to better understand the conditions that lead to the HABs and to predict when they will occur. Nutrient management strategies such as mulch tillage may be the most applicable to the Skaneateles Lake Watershed to mitigate pollution from agricultural fields. Riparian buffers will help to protect from any other sources of nutrients that may reach the lake. There are physical, chemical, and biological methods to control invasive species in Skaneateles Lake, and reducing these invasive populations will help to reduce HABs by reducing nutrient loading and increasing competition of other microorganisms. The problem of HABs is multifaceted, and strong coordination and responsibility between government agencies, farmers, and citizens of the Skaneateles Lake Watershed will need to be enforced and encouraged to hope for long-term reduction in HABs.
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