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Nitrogen limitation, toxin synthesis potential, and toxicity of cyanobacterial populations in Lake Okeechobee and the St. Lucie River Estuary, Florida, during the 2016 state of emergency event

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Lake Okeechobee, FL, USA, has been subjected to intensifying cyanobacterial blooms that can spread to the adjacent St. Lucie River and Estuary via natural and anthropogenically-induced flooding events. In July 2016, a large, toxic cyanobacterial bloom occurred in Lake Okeechobee and throughout the St. Lucie River and Estuary, leading Florida to declare a state of emergency. This study reports on measurements and nutrient amendment experiments performed in this freshwater-estuarine ecosystem (salinity 0–25 PSU) during and after the bloom. In July, all sites along the bloom exhibited dissolved inorganic nitrogen-to-phosphorus ratios < 6, while Microcystis dominated (> 95%) phytoplankton inventories from the lake to the central part of the estuary. Chlorophyll a and microcystin concentrations peaked (100 and 34 μg L⁻¹, respectively) within Lake Okeechobee and decreased eastwards. Metagenomic analyses indicated that genes associated with the production of microcystin (mcyE) and the algal neurotoxin saxitoxin (sxtA) originated from Microcystis and multiple diazotrophic genera, respectively. There were highly significant correlations between levels of total nitrogen, microcystin, and microcystin synthesis gene abundance across all surveyed sites (p < 0.001), suggesting high levels of nitrogen supported the production of microcystin during this event. Consistent with this, experiments performed with low salinity water from the St. Lucie River during the event indicated that algal biomass was nitrogen-limited. In the fall, densities of Microcystis and concentrations of microcystin were significantly lower, green algae co-dominated with cyanobacteria, and multiple algal groups displayed nitrogen-limitation. These results indicate that monitoring and regulatory strategies in Lake Okeechobee and the St. Lucie River and Estuary should consider managing loads of nitrogen to control future algal and microcystin-producing cyanobacterial blooms.
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... While this study is one of few to connect downstream HABs with upstream nutrient loading from septic systems, this has been observed in other locations, such as the St. Lucie Estuary, FL (Lapointe et al., 2017), Waquoit Bay, Massachusetts (Valiela et al., 1992) and Lake Huron, Ontario, Canada (Rakhimbekova et al., 2021). In many areas of Florida, due to the high background P (Odum, 1953), N has been identified as the element most capable of promoting algal growth and toxicity-especially for cyanobacteria (Kramer et al., 2018), which has been observed in other locations as well (Gobler et al., 2016). In the estuarine and coastal environments adjacent to Lee County, M. aeruginosa and K. brevis blooms thrive in low N:P conditions (Ketchum and Keen, 1948;Odum, 1953;Lapointe et al., 2006;Yentsch et al., 2008;Lapointe et al., 2012;Lapointe et al., 2017), but K. brevis can also be sustained at higher N:P (Odum et al., 1955). ...
... During wet periods, such as following tropical storms or hurricanes, the downstream Caloosahatchee River Estuary can be seeded with M. aeruginosa from Lake Okeechobee freshwater discharges. Similarly, blooms of M. aeruginosa occurred in Southeast Florida's St. Lucie River Estuary in 2005, 2013, and 2016 that were attributed to algal "seeding" from Lake Okeechobee discharges combined with high biomass local basin blooms supported by urban nutrient loading (Lapointe et al., 2012;Phlips et al., 2012;Lapointe et al., 2017;Kramer et al., 2018). In 2016, the phytoplankton biomass in Lake Okeechobee was N-limited during M. aeruginosa bloom conditions (Kramer et al., 2018); thus after heavy rainfall and discharges these blooms experienced exponential growth in urbanized estuaries with low salinities and high levels of DIN, especially NH 4 + (Lapointe et al., 2017;Kramer et al., 2018). ...
... Similarly, blooms of M. aeruginosa occurred in Southeast Florida's St. Lucie River Estuary in 2005, 2013, and 2016 that were attributed to algal "seeding" from Lake Okeechobee discharges combined with high biomass local basin blooms supported by urban nutrient loading (Lapointe et al., 2012;Phlips et al., 2012;Lapointe et al., 2017;Kramer et al., 2018). In 2016, the phytoplankton biomass in Lake Okeechobee was N-limited during M. aeruginosa bloom conditions (Kramer et al., 2018); thus after heavy rainfall and discharges these blooms experienced exponential growth in urbanized estuaries with low salinities and high levels of DIN, especially NH 4 + (Lapointe et al., 2017;Kramer et al., 2018). This is consistent with this study, where cyanobacterial bloom samples collected from nearby Cape Coral residential canals (Fig. S2) (Lapointe and Bedford, 2007;Dixon et al., 2014;Heil et al., 2014), which could have implications for bloom development. ...
Article
As human population growth has expanded in Southwest Florida, water quality has become degraded with an increased occurrence of harmful algal blooms (HABs). Red tide (Karenia brevis) originating offshore, intensifies in nearshore waters along Florida's Gulf Coast, and blue-green algae (Microcystis spp.) originating in Lake Okeechobee is discharged into the Caloosahatchee River. These HABs could be enhanced by anthropogenic nitrogen (N) and phosphorus (P) from adjacent watersheds. North Fort Myers is a heavily developed, low-lying city on the Caloosahatchee River Estuary serviced by septic systems with documented nutrient and bacterial pollution. To identify sources of pollution within North Fort Myers and determine connections with downstream HABs, this multiyear (2017–2020) study examined septic system- groundwater- surface water couplings through the analysis of water table depth, nutrients (N, P), fecal indicator bacteria (FIB), molecular markers (HF183, GFD, Gull2), chemical tracers (sucralose, pharmaceuticals, herbicides, pesticides), stable isotopes of groundwater (δ¹⁵N-NH4, δ¹⁵N-NO3) and particulate organic matter (POM; δ¹⁵N, δ¹³C), and POM elemental composition (C:N:P). POM samples were also collected during K. brevis and Microcystis spp. HAB events. Most (>80%) water table depth measurements were too shallow to support septic system functioning (<1.07 m). High concentrations of NH4⁺ and NOx, up to 1094 μM and 482 μM respectively, were found in groundwater and surface waters. δ¹⁵N values of groundwater (+4.7‰) were similar to septic effluent (+4.9‰), POM (+4.7‰), and downstream HABs (+4.8 to 6.9‰), indicating a human waste N source. In surface waters, FIB were elevated and HF183 was detected, while in groundwater and surface waters sucralose, carbamazepine, primidone, and acetaminophen were detected. These data suggest that groundwater and surface water in North Fort Myers are coupled and contaminated by septic system effluent, which is negatively affecting water quality and contributing to the maintenance and intensification of downstream HABs.
... A diverse array of cyanobacterial species have been documented from many Florida waters, including freshwater springs, ponds and lakes, rivers, estuaries and marine environments. Increasingly, toxic cyanoHABs and/or their toxins are being documented in additional freshwater systems within the state, including the St John's River (Havens et al., 2019;Landsberg et al., 2020), Lake Okeechobee (Havens et al., 2003;Kramer et al., 2018), the St. Lucie River (Kramer et al., 2018) and the Caloosahatchee River (Metcalf et al., 2021) as well as some estuarine and marine environments within Florida Tiling and Proffitt, 2017;Lefler et al., 2021;Metcalf et al., 2021). These freshwater and marine cyanoHABs are not necessarily separate events. ...
... A diverse array of cyanobacterial species have been documented from many Florida waters, including freshwater springs, ponds and lakes, rivers, estuaries and marine environments. Increasingly, toxic cyanoHABs and/or their toxins are being documented in additional freshwater systems within the state, including the St John's River (Havens et al., 2019;Landsberg et al., 2020), Lake Okeechobee (Havens et al., 2003;Kramer et al., 2018), the St. Lucie River (Kramer et al., 2018) and the Caloosahatchee River (Metcalf et al., 2021) as well as some estuarine and marine environments within Florida Tiling and Proffitt, 2017;Lefler et al., 2021;Metcalf et al., 2021). These freshwater and marine cyanoHABs are not necessarily separate events. ...
... These freshwater and marine cyanoHABs are not necessarily separate events. Some toxic freshwater cyanobacterial blooms, along with their toxins (e.g., toxic Microcystis blooms in Lake Okeechobee), are being transferred to estuarine and coastal waters (Oehrle et al., 2017;Metcalf et al., 2021;Tatters et al., 2021) through water management actions (Kramer et al., 2018), a trend for cyanoHABs that is occurring globally (Preece et al., 2017). Metcalf et al. (2021) reports that during analysis of a co-occurring 2018 bloom of Microcystis spp. in Lake Okeechobee and Karenia brevis in the Gulf of Mexico, brevetoxin was detected at low salinities (0.4 mS cm −1 ) and microcystin-LR at higher salinities (41 mS cm −1 ), indicating that there may be synergistic effects of co-occurring toxins at the freshwater-marine interface. ...
... For many decades, Lake Okeechobee, and its modified rivers (Caloosahatchee River and St. Lucie River) have been subjected to intensifying Microcystis aeruginosa bloom events, especially during the wet season when temperatures are high and nutrient loadings are prominent (Kramer et al. 2018). The high loading of nutrients from the watersheds and the discharge of water from Lake Okeechobee through the C-44 (St. ...
... The high loading of nutrients from the watersheds and the discharge of water from Lake Okeechobee through the C-44 (St. Lucie River) and the C-43 canals has been speculated as a major cause of a widespread blooms in estuaries at both coasts (Kramer et al. 2018). The most recent bloom event occurred in the Caloosahatchee River in 2018 led to a declaration of a state of emergency in Florida due to social-economic and health impacts. ...
... There was a strong positive correlation (R = 0.6, P = 0.001, n = 26) between chlorophyll a and total iron concentrations in the samples and that over half of and Reddy 1995;Aumen 1998). For many decades, Lake Okeechobee has been reported as being subjected to intensifying M. aeruginosa bloom events, especially during the wet season when temperatures are high and nutrient loading is prominent (Kramer et al. 2018). The high loading of nutrients from the watershed and the discharge of water from Lake Okeechobee through the C-44 (St. ...
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Hydrogen peroxide is widely recognized as the most stable of the reactive oxygen species (ROS) produced by abiotic, biotic and sediments in natural waters. By mediating redox transformations, hydrogen peroxide may directly or indirectly affect aquatic ecosystems. It might be particularly important in the biology and ecology of harmful freshwater cyanobacteria blooms which are increasingly occurring in nutrient-rich freshwater bodies. Environmental interactions between cyanobacteria and natural hydrogen peroxide could play a large role in cyanobacterial blooms, but little is known about these interactions. To better understand the interactions of hydrogen peroxide and cyanobacteria, we determined the hydrogen peroxide level in the presence and absence of cyanobacterial blooms. Also, we aimed to understand the ecological significance of hydrogen peroxide production by cyanobacteria in the waters of southwest Florida, a subtropical zone which experiences strong sunlight and heavy precipitations in the rainy season. In this study, hydrogen peroxide concentrations were determined using a fast response amperometric hydrogen peroxide microsensor in 24 freshwater bodies. Our results indicated that rainwater contains higher hydrogen peroxide levels (0-92.9 µM) than freshwater bodies under cyanobacterial bloom conditions (0-5.3 µM). To determine the potential biodegradation of hydrogen peroxide during sample transportation in the dark (opaque containers), water samples were passed through 0.2 µm filters immediately after sampling and compared with unfiltered water samples in the laboratory. We found the filtered water samples retained higher concentrations of hydrogen peroxide than non-filtered samples; and we determined the mean biodegradation rate of hydrogen peroxide was 44.7 ±10.6 nmol/h in unfiltered water. We also determined the baseline hydrogen peroxide concentrations and microscale depth profiles (10-60 mm) of hydrogen peroxide using a recently developed hydrogen peroxide microsensor. The hydrogen peroxide concentrations were higher at M. aeruginosa bloom sites compared to control sites and higher in locations exposed to sunlight than in shaded locations. In addition, micro-profiles showed extremely high hydrogen peroxide concentrations (3.3 to 20.9 µM) in the uppermost layer of the lake water in cyanobacterial blooms. All together, we found hydrogen peroxide hotspots in fresh waterbodies in a subtropical region that were generated by both abiotic and biotic factors. In addition, we found extremely high hydrogen peroxide concentrations in cyanobacterial bloom sites compared to reported values from other freshwater systems which could have a large effect on the aquatic microbial community.
... Ecological, biochemical, and flow regime studies of the St. Lucie Estuary Basin have improved the knowledge base of best management practices [25, [29][30][31] and eutrophication science [32][33][34][35]. Studies by Doering (1996) [29] and Chamberlain and Hayward (1996) [26] recommended a more stable, lower flow from canals to improve water quality and attain resource management goals. ...
... Qian et al. (2007) [30] assessed long-term data (1979 to 2004) of water quality constituents in major canals and found that almost all nutrient species had significantly higher concentrations in the wet than in the dry season. Studies by Hampel et al. (2020) [32], Kramer et al. (2018) [33], and Oehrle et al. (2017) [35] demonstrated the key role of nitrogen species and salinity in toxic Microcystis blooms in the lakeestuary continuum. The South Florida Water Management District (SFWMD) and the Florida Department of Environmental Protection (FDEP) continuously assess the water quality of the estuary and the lake. ...
... Qian et al. (2007) [30] assessed long-term data (1979 to 2004) of water quality constituents in major canals and found that almost all nutrient species had significantly higher concentrations in the wet than in the dry season. Studies by Hampel et al. (2020) [32], Kramer et al. (2018) [33], and Oehrle et al. (2017) [35] demonstrated the key role of nitrogen species and salinity in toxic Microcystis blooms in the lakeestuary continuum. The South Florida Water Management District (SFWMD) and the Florida Department of Environmental Protection (FDEP) continuously assess the water quality of the estuary and the lake. ...
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Anthropogenic developments in coastal watersheds cause significant ecological changes to estuaries. Since estuaries respond to inputs on relatively long time scales, robust analyses of long-term data should be employed to account for seasonality, internal cycling, and climatological cycles. This study characterizes the water quality of a highly managed coastal basin, the St. Lucie Estuary Basin, FL, USA, from 1999 to 2019 to detect spatiotemporal differences in the estuary's water quality and its tributaries. The estuary is artificially connected to Lake Okeechobee, so it receives fresh water from an external basin. Monthly water samples collected from November 1999 to October 2019 were assessed using principal component analysis, correlation analysis, and the Seasonal Kendall trend test. Nitrogen, phosphorus, color, total suspended solids, and turbidity concentrations varied seasonally and spatially. Inflows from Lake Okeechobee were characterized by high turbidity, while higher phosphorus concentrations characterized inflows from tributaries within the basin. Differences among tributaries within the basin may be attributed to flow regimes (e.g., significant releases vs. steady flow) and land use (e.g., pasture vs. row crops). Decreasing trends for orthophosphate, total phosphorus, and color and increasing trends for dissolved oxygen were found over the long term. Decreases in nutrient concentrations over time could be due to local mitigation efforts. Understanding the differences in water quality between the tributaries of the St. Lucie Estuary is essential for the overall water quality management of the estuary.
... The dominant species often undergoes succession under changing environmental conditions (e.g., precipitation, temperature, light intensity, salinity, dissolved CO 2 , nutrients, iron, alkalinity), which favor growth and persistence of particular species over others. These same abiotic factors (e.g., both limitation and/or abundance of phosphorous or nitrogen, pH, salinity) influence the production and secretion of toxins by harmful phytoplankton in complex ways (e.g., Errera et al., 2008;Hambright et al., 2014;Horst et al., 2014;Johansson and Granéli, 1999;Kramer et al., 2018;Pimentel and Giani, 2014;Roelke et al., 2016;Shilo and Aschner, 1953;Wilhelm et al., 2020;Wood et al., 2011). Toxicity may be additionally influenced by biotic ecosystem interactions, where stress-inducing predation/parasitism initiates toxin production (e.g., Jang et al., 2003;Mitra and Flynn, 2006;Tillmann, 2003). ...
... CyanoHABs occur primarily in lentic systems. However, bloomforming species and their associated cyanotoxins can be found throughout entire watersheds, from first-order wadeable streams (Fetscher et al., 2015), to large rivers downstream of infected impounded waters (e.g., Otten et al., 2015), and finally to river outlets in brackish estuaries (e.g., Kramer et al., 2018;Lehman et al., 2005;Otten et al., 2017;Peacock et al., 2018). Even here, at the freshwater-saltwater interface, widespread cyanoHABs are known to occur. ...
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Recurrence and severity of harmful algal blooms (HABs) are increasing due to a number of factors, including human practices and climate change. Sensitive and robust methods that allow for early and expedited HAB detection across large landscape scales are needed. Among the suite of HAB detection tools available, a powerful option exists in genetics-based approaches utilizing environmental sampling, also termed environmental DNA (eDNA). Here we provide a detailed methodological review of three HAB eDNA approaches (quantitative PCR, high throughput sequencing, and isothermal amplification). We then summarize and synthesize recently published eDNA applications covering a variety of HAB surveillance and research objectives, all with a specific emphasis in the detection of two widely problematic freshwater species, Microcystis aeruginosa and Prymnesium parvum. In our summary and conclusion we build on this literature by discussing ways in which eDNA methods could be advanced to improve HAB detection. We also discuss ways in which eDNA data could be used to potentially provide novel insight into the ecology, mitigation, and prediction of HABs.
... These toxins can affect the skin, liver, kidneys, reproductive system, and central nervous system (USEPA, 2014;Wilde et al., 2014;Breinlinger et al., 2021). The significant impact of cyanoHABs is exemplified by large-scale bloom events such as the drinking water supply crisis in Lake Erie (Obenour et al., 2014;Bertani et al., 2016) and Lake Okeechobee (Kramer et al., 2018). In addition, cyanobacteria blooms harm the economy by causing fishery closures, limiting access to recreation areas, and affecting housing values for shoreline communities (Graham et al., 2017). ...
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Reservoirs are dominant features of the modern hydrologic landscape and provide vital services. However, the unique morphology of reservoirs can create suitable conditions for excessive algae growth and associated cyanobacteria blooms in shallow in-flow reservoir locations by providing warm water environments with relatively high nutrient inputs, deposition, and nutrient storage. Cyanobacteria harmful algal blooms (cyanoHAB) are costly water management issues and bloom recurrence is associated with economic costs and negative impacts to human, animal, and environmental health. As cyanoHAB occurrence varies substantially within different regions of a water body, understanding in-lake cyanoHAB spatial dynamics is essential to guide reservoir monitoring and mitigate potential public exposure to cyanotoxins. Cloud-based computational processing power and high temporal frequency of satellites enables advanced pixel-based spatial analysis of cyanoHAB frequency and quantitative assessment of reservoir headwater in-flows compared to near-dam surface waters of individual reservoirs. Additionally, extensive spatial coverage of satellite imagery allows for evaluation of spatial trends across many dozens of reservoir sites. Surface water cyanobacteria concentrations for sixty reservoirs in the southern U.S. were estimated using 300 m resolution European Space Agency (ESA) Ocean and Land Colour Instrument (OLCI) satellite sensor for a five year period (May 2016–April 2021). Of the reservoirs studied, spatial analysis of OLCI data revealed 98% had more frequent cyanoHAB occurrence above the concentration of >100,000 cells/mL in headwaters compared to near-dam surface waters (P < 0.001). Headwaters exhibited greater seasonal variability with more frequent and higher magnitude cyanoHABs occurring mid-summer to fall. Examination of reservoirs identified extremely high concentration cyanobacteria events (>1,000,000 cells/mL) occurring in 70% of headwater locations while only 30% of near-dam locations exceeded this threshold. Wilcoxon signed-rank tests of cyanoHAB magnitudes using paired-observations (dates with observations in both a reservoir's headwater and near-dam locations) confirmed significantly higher concentrations in headwater versus near-dam locations (p < 0.001).
... Additionally, increased atmospheric inputs during the wet season could also lower δ 15 N values (Paerl and Fogel, 1994). The surface water DIN:SRP was significantly lower in the wet season, which could create ideal conditions for nitrogen fixers (Glibert and Burkholder, 2011;Lapointe et al., 2015Lapointe et al., , 2017Kramer et al., 2018). Surface water δ 15 N-NO 3 − values were significantly lower in the wet season, indicating that less nitrification/denitrification is occurring prior to discharge of NO 3 − from the groundwater, likely due to increased mobilization by rainfall. ...
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Effluent from septic systems can pollute groundwater and surface waters in coastal watersheds. These effects are unknown for the highly urbanized central Indian River Lagoon (CIRL), Florida, where septic systems represent > 50% of wastewater disposal. To better understand these impacts, water quality was assessed along both canals and a tributary that drain into the CIRL. Dissolved nutrient concentrations were higher near septic systems than in natural areas. δ¹⁵N values of groundwater (+7.2‰), surface water (+5.5‰), and macrophytes (+9.7‰) were within the range for wastewater (>+3‰), as were surface water concentrations of the artificial sweetener sucralose (100 to 1700 ng/L) and fecal indicator bacteria density. These results indicate that septic systems are promoting eutrophication in the CIRL by contributing nutrient pollution to surface water via groundwater. This study demonstrates the need to reduce reliance on septic systems in urbanized coastal communities to improve water quality and subsequently mitigate harmful algal blooms.
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