Marine Biology (2019) 166:108 https://doi.org/10.1007/s00227-019-3538-9 HIGHLIGHT ARTICLE Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: a 3-decade study Brian E. Lapointe1 · Rachel A. Brewton1 · Laura W. Herren1 · James W. Porter2 · Chuanmin Hu3 Received: 8 February 2019 / Accepted: 3 June 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Increased loadings of nitrogen (N) from fertilizers, top soil, sewage, and atmospheric deposition are important drivers of eutrophication in coastal waters globally. Monitoring seawater and macroalgae can reveal long-term changes in N and phosphorus (P) availability and N:P stoichiometry that are critical to understanding the global crisis of coral reef decline. Analysis of a unique 3-decade data set for Looe Key reef, located offshore the lower Florida Keys, showed increased dis- solved inorganic nitrogen (DIN), chlorophyll a, DIN:soluble reactive phosphorus (SRP) ratios, as well as higher tissue C:P and N:P ratios in macroalgae during the early 1990s. These data, combined with remote sensing and nutrient monitoring between the Everglades and Looe Key, indicated that the significant DIN enrichment between 1991 and 1995 at Looe Key coincided with increased Everglades runoff, which drains agricultural and urban areas extending north to Orlando, Florida. This resulted in increased P limitation of reef primary producers that can cause metabolic stress in stony corals. Outbreaks of stony coral disease, bleaching, and mortality between 1995 and 2000 followed DIN enrichment, algal blooms, and increased DIN:SRP ratios, suggesting that eutrophication interacted with other factors causing coral reef decline at Looe Key. Although water temperatures at Looe Key exceeded the 30.5 °C bleaching threshold repeatedly over the 3-decade study, the three mass bleaching events occurred only when DIN:SRP ratios increased following heavy rainfall and increased Everglades runoff. These results suggest that Everglades discharges, in conjunction with local nutrient sources, contributed to DIN enrichment, eutrophication, and increased N:P ratios at Looe Key, exacerbating P limitation, coral stress and decline. Improved manage- ment of water quality at the local and regional levels could moderate N inputs and maintain more balanced N:P stoichiometry, thereby reducing the risk of coral bleaching, disease, and mortality under the current level of temperature stress. Introduction have been in decline globally since the 1970s due to a grow- ing number of recognized stressors (Hughes et al. 2003; Coral reefs have evolved over hundreds of millions of years Wilkinson 2004). In the Caribbean basin, an estimated 40% and are now considered one of the most threatened eco- of coral has been lost over the last 40 years (Gardner et al. systems on our planet (Birkeland 1997, 2004; MEA 2005; 2003) and similar losses have been observed along the Great Hughes et al. 2017). These biologically diverse ecosystems Barrier Reef, Australia (Bellwood et al. 2004; De’ath et al. 2012). Early studies focused largely on the effects of land- based nutrient pollution and eutrophication (Banner 1974; Responsible Editor: S. Shumway. Tomascik and Sander 1987; Smith et al. 1981; Bell 1992; Lapointe and Clark 1992), which was considered a primary Reviewed by undisclosed experts. threat to coral reef health in the late 1980s (NOAA 1988; * Brian E. Lapointe Ginsburg 1994). Since then, overfishing (Hughes 1994; [email protected] Jackson et al. 2001), sedimentation (Rogers 1990; Fab- ricius 2005), increases in sea surface temperature (Goreau 1 Harbor Branch Oceanographic Institute, Florida Atlantic and Hayes 1994; Glynn 1996; Baker et al. 2008; Selig et al. University, 5600 US-1, Fort Pierce, FL 34946, USA 2012; Hughes et al. 2017), and ocean acidification (Kley- 2 Odum School of Ecology, University of Georgia, Athens, pas et al. 2006; Hoegh-Guldberg et al. 2007; Muehllehner GA 30602, USA et al. 2016) have emerged as additional threats to coral reefs. 3 College of Marine Science, University of South Florida, While the potential for negative impacts (both direct and St. Petersburg, FL 33701, USA Vol.:(0123456789)1 3 108 Page 2 of 31 Marine Biology (2019) 166:108 indirect) to coral reefs from nutrient enrichment remains a Nitrogen enrichment can also increase the prevalence of major issue (Fabricius 2005; D’Angelo and Wiedenmann coral diseases (Bruno et al. 2003; Voss and Richardson 2014), the synergistic effects of anthropogenic stressors 2006; Vega-Thurber et al. 2014; Rädecker et al. 2015; Wang combined with climate change have the capacity to cause et al. 2018), further accelerating coral mortality. the greatest damage (Wilkinson 1996; Anthony et al. 2011; Altered ecological stoichiometry associated with increas- Zaneveld et al. 2016; Wang et al. 2018). ing N loading from human activities (Vitousek et al. 1997; Nitrogen (N) enrichment, a driver of eutrophication and Sterner and Elser 2002; Rockström et al. 2009) can impart global change in the marine environment (Ryther and Dun- direct physiological effects on corals, leading to a disruption stan 1971; NRC 2000; MEA 2005), has long been known in the control of endosymbiotic zooxanthellae (Falkowski as a stressor to coral reefs (Smith et al. 1981; Tomascik and et al. 1993; Dubinsky and Stambler 1996). Dissolved inor- Sander 1985; Bell 1992; Lapointe and Clark 1992; Fabricius ganic nitrogen (DIN = ammonium + nitrate) enrichment 2005; Duprey et al. 2016). The issue of N enrichment to controls the growth of endosymbiotic zooxanthellae (D’Elia coral health is related to the paradox that highly produc- et al. 1991; Falkowski et al. 1993; Fagoonee et al. 1999), tive coral reefs thrive under oligotrophic conditions (Darwin and increased endosymbiont densities result in a greater sus- 1842). In their classic studies at Enewetak Atoll, Odum and ceptibility to coral bleaching (Cunning and Baker 2013). Odum (1955) concluded that coral reef ecosystems have a Elevated DIN without a balanced supply of soluble reactive high efficiency of phosphorus (P) cycling, which has been phosphorus (low SRP concentrations and/or high N:P ratio) confirmed by subsequent studies (Pilson and Betzer 1973; can induce P starvation in corals, effectively reducing the Atkinson 1987). Corals are adapted to thrive at low nutri- temperature and light thresholds for bleaching (Wooldridge ent levels typical of oligotrophic tropical waters because of 2009; Wiedenmann et al. 2013; D’Angelo and Wiedenmann tight internal nutrient cycling by endosymbiotic zooxanthel- 2014; Rosset et al. 2017). Much remains to be understood lae (D’Elia and Webb 1977; Muscatine and Porter 1977; about how human activities on watersheds of coral reefs are O’Neil and Capone 2008). Odum and Odum (1955) sug- altering the relative availability of N and P to coastal waters, gested that N was the limiting nutrient for coral reef com- and how these changes relate to the growing problem of munities and that N2 fixation by cyanobacteria helped to mass coral bleaching, disease, and mortality. meet the N demands necessary to sustain the high gross Recognition of the paramount importance of water productivity of coral reefs. Indeed, cyanobacteria on reef quality to the health of coral reefs in the Florida Keys led flats at Enewetak Atoll fixed N 2 at high rates, helping to to its designation as an “Area of Critical State Concern” explain the high productivity of adjacent coral reefs (Wiebe by the Florida Legislature in 1974 (Table 1). Following et al. 1975). More recent studies using δ15N indicated that the first reports of coral reef decline off Key Largo in the some great star coral Montastraea cavernosa colonies also 1970s (Dustan 1977; Dustan and Halas 1987) and the role contain endosymbiotic cyanobacterial N2 fixers (Lesser et al. of septic systems in contributing to nearshore eutrophi- 2007), although coral–diazotrophic interactions are complex cation (Lapointe et al. 1990), nutrient pollution became (Rädecker et al. 2015). a primary issue in the Florida Keys. In 1988, 50 coral Considering the contribution of N 2 fixation to the high reef experts met at a National Oceanic and Atmospheric productivity of coral reefs, this relationship could be altered Administration (NOAA)-sponsored workshop in Key by increases in external N inputs from human activities Largo, Florida and ranked various problems affecting the (Vitousek et al. 1997). Increased anthropogenic N load- coral reefs of the Florida Keys; the primary conclusion ing has had major ecological consequences for coral reefs, was “excessive amounts of nutrients invading the Florida including increased phytoplankton blooms (Caperon et al. Reef Tract from the Keys and from Florida Bay are a seri- 1976; Laws and Redalje 1979, 1982; Smith et al. 1981; Bell ous and widespread problem” (NOAA 1988; Table 1). 1992; Yentsch et al. 2002) that reduce light and accelerate Therefore, deterioration of water quality was a primary coral reef decline (Tomascik and Sander 1985; Hallock and factor leading to the passage of the Florida Keys National Schlager 1986; Fabricius et al. 2016). Experimental field Marine Sanctuary (FKNMS) Act in 1990, which mandated studies have shown myriad ecological effects of increas- a multi-agency Water Quality Protection Program (WQPP; ing N enrichment, such as enhanced growth of macroalgae Table 1) consisting of NOAA, the United States Environ- (Smith et al. 1981; Lapointe 1997; Smith et al. 2007; De’ath mental Protection Agency (US EPA), and the Florida and Fabricius 2010; Lapointe et al. 2011) and algal turfs Department of Environmental Protection (FDEP). The (Hatcher and Larkum 1983; Williams and Carpenter 1988; WQPP was the first of its kind for a United States marine Vermeij et al. 2010), which can inhibit coral recruitment sanctuary (NOAA 1996; Kruczynski and McManus 2002). and outcompete corals for space (Birkeland 1977; River The boundaries of the FKNMS extended from northern and Edmunds 2001; Nugues et al. 2004; Vega-Thurber et al. Key Largo to the Dry Tortugas, encompassing an area of 2012; O’Brien and Scheibling 2018; Pratte et al.