Short Term Effects of Hurricane Irma and Cyanobacterial Blooms on Ammonium Cycling Along a Freshwater–Estuarine Continuum in South Florida

Abstract

Lacustrine and coastal systems are vulnerable to the increasing number and intensity of tropical storms driven by climate change. Strong winds associated with tropical storms can mobilize nutrients in sediments and alter nitrogen and phosphorus cycling, leading to amplification of preexisting conditions, such as eutrophication and cyanobacterial blooms (cyanoHABs). In 2016, Florida declared a State of Emergency within and downstream of Lake Okeechobee (LO) due to toxic cyanobacterial blooms (primarily Microcystis). The blooms originated in LO, but flood control measures released water from LO to the brackish St. Lucie Estuary (SLE). In September 2017, Hurricane Irma traversed the Florida peninsula with sustained winds exceeding 160 km h −1 , generating torrential rains over the watershed. We quantified ammonium (NH + 4) regeneration and potential uptake rates, and Microcystis toxin gene (mcyD) abundance in LO and SLE during the massive bloom in July 2016, the bloom in August 2017 (2 weeks before Irma), and 10 days after Hurricane Irma landfall. In 2016, cyanoHABs were present in both LO and SLE, and potential NH + 4 uptake rates were high in both systems. In 2017, the bloom was constrained to LO, potential NH + 4 uptake rates in LO exceeded those in SLE, and mcyD gene abundance was greater in LO than SLE. Post Hurricane Irma, potential NH + 4 uptake rates decreased significantly in LO and SLE, while mcyD gene abundance decreased in LO and increased slightly in SLE. Average NH + 4 regeneration rates could support 25-40% of water column potential NH + 4 demand in the lake and, when extrapolated to the entire LO water column, exceeded external nitrogen loading. These results emphasize the importance of internal NH + 4 recycling for bloom expansion and toxicity in the lake and downstream estuaries. In 2018, the cyanobacterial bloom in the Okeechobee region was one of the largest recorded and is presumed to be driven by the aftermath of Hurricane Irma. Large-scale blooms have also been observed in SLE, likely due to LO flushing and decreased salinity post-hurricane. Thus, results from this study support predictions that increased frequency and strength of tropical storms will lead to more intense blooms in aquatic systems.

Hurricane Disturbance Stimulated Nitrification and Altered Ammonia Oxidizer Community Structure in Lake Okeechobee and St. Lucie Estuary (Florida)

“…Nitrification rates in Lake Okeechobee were low during cyanoHABs in 2016 and 2017 (Figure 2A), similar in magnitude to those from oligotrophic Lake Superior (Small et al, 2013), and lower than those previously measured in spring in Lake Okeechobee (James et al, 2009). Competition for NH 4 + between nitrifiers and photoautotrophs, including cyanobacteria, may inhibit nitrification during severe cyanoHABs, which were observed in Lake Okeechobee in 2016 (Kramer et al, 2018;Hampel et al, 2019). NH 4 + is the most energetically favorable N form for primary producers, including non-N 2 fixing cyanobacteria (e.g., Microcystis), which often outcompete other algal groups (e.g., Blomqvist et al, 1994) and ammonia oxidizers for NH 4 + .…”

“…Undetectable and low nitrification rates in the upstream estuary are likely due to the presence of cyanoHABs during sampling and increased competition for NH 4 + . High photoautotrophic NH 4 Hampel et al, 2019), coincident with high Microcystis cell densities in the upstream estuary (Kramer et al, 2018), suggest that nitrifiers were outcompeted for FIGURE 6 | Phylogenetic tree of ammonia-oxidizing archaea OTUs classified from amoA reads at 95% similarity with reference sequences (Alves et al, 2018). OTU label colors indicate OTUs found in Lake Okeechobee (green), St. Lucie Estuary (blue), or both systems (black).…”

“…+ uptake rates and microcystin synthetase gene abundance (Hampel et al, 2019). Previous studies showed decreased AOA abundance and diversity after an oil spill (Newell et al, 2014) and increased AOB abundance after storm disturbance (Happel et al, 2018).…”

“…Environmental data have been reported previously (Hampel et al, 2019) and are presented here in Supplementary Tables S1, S2. Water temperature in the lake and estuary was uniform across all sampling events.…”

“…On September 10th, 2017, Hurricane Irma made landfall in the Florida Keys as a Category 4 hurricane (sustained winds >210 km h −1 ) and moved through central Florida with sustained winds of ∼65 km h −1 in the Okeechobee region (Hampel et al, 2019) and maximum winds up to ∼100 km h −1 (SFWMD). High winds and precipitation runoff have major impacts on hydrology, microbial and phytoplankton community structure, sediments, and nutrients, including reducing salinity in estuaries, often leading to stratification and bottom-water hypoxia (Paerl et al, 2001).…”