Harmful Algae 43 (2015) 82–102 Contents lists available at ScienceDirect Harmful Algae jo urnal homepage: www.elsevier.com/locate/hal Evidence of sewage-driven eutrophication and harmful algal blooms in Florida’s Indian River Lagoon Brian E. Lapointe *, Laura W. Herren, David D. Debortoli, Margaret A. Vogel Harbor Branch Oceanographic Institute at Florida Atlantic University, Harmful Algal Bloom Program, 5600 US 1 North, Fort Pierce, FL 34946, USA A R T I C L E I N F O A B S T R A C T Article history: Nutrient pollution is a primary driver of eutrophication and harmful algal blooms (HABs) in estuaries and Received 17 October 2014 coastal waters worldwide. In 2011–2012, 20 sites evenly distributed throughout the 251-km long Indian Received in revised form 27 January 2015 River Lagoon (IRL) were assessed during three sampling events for dissolved nutrients (DIN, SRP, TDN, Accepted 28 January 2015 13 15 TDP) and chlorophyll a. Benthic macroalgae were also analyzed for d C, d N, and C:N:P contents to identify potential nutrient sources and gauge the type and degree of N and P limitation. The mean DIN Keywords: and SRP concentrations throughout the IRL were high, averaging 4.24 Æ 0.45 and 0.68 Æ 0.06 mM, HAB respectively, explaining the widespread occurrence of HABs during the study. High TDN concentrations (up Nitrogen to 152 M) and TDN:TDP ratios (>100:1) in the poorly flushed northern IRL, Mosquito Lagoon and Banana Phosphorus m River segments reflected the accumulation and cycling of N-rich groundwater inputs that produce P- Indian River Lagoon Eutrophication limitation. These enriched nutrient conditions were associated with unprecedented chlorophyll a Stable isotopes concentrations (>100 mg/L), dominated by Resultor sp. Ø. Moestrup in the Banana River in 2011 and Aureoumbra lagunensis D.A. Stockwell, DeYoe, Hargraves and P.W. Johnson in the Mosquito Lagoon and northern IRL in 2012. C:N, C:P, and N:P ratios in macroalgae averaged 15.9, 698.9, and 40.6, throughout the IRL, respectively; significantly higher C:P and N:P ratios in the northern IRL segments suggested strong P- 15 limitation in these N-enriched waters. Macroalgae d N values were enriched throughout the IRL (+6.3%) and similar to values reported for macroalgae from other sewage-polluted coastal waters. Because point- source sewage inputs to the IRL were largely eliminated through the IRL Act of 1990, these results suggest that non-point source N enrichment from septic tanks (300,000) represents a significant and largely ignored N-source to the IRL. The high degree of sewage N contamination of the IRL, combined with recent HABs, including toxic ecotypes of the red macroalga Gracilaria tikvahiae McLachlan, seagrass loss, and wildlife mortality, indicates a critical need for improved sewage collection and treatment, including nutrient removal. ß 2015 Elsevier B.V. All rights reserved. 1. Introduction of global change in coastal waters, linking an array of problems along coastlines, including eutrophication, biodiversity loss, Coastal and estuarine ecosystems are among the most harmful algal blooms (HABs), ‘‘dead zones,’’ emerging marine productive ecosystems in the world, providing invaluable ecologi- diseases, fish kills, and loss of seagrass and coral reef ecosystems cal services to human populations. However, many of these (NRC, 2000; Howarth and Marino, 2006; Rockstro¨m et al., 2009). ecosystems are being degraded as a result of expanding human Located along Florida’s east-central coast, the Indian River activities such that their ability to sustain future societal needs is Lagoon (IRL) is a shallow (mean depth 0.8 m) and narrow (3 km now at risk. Humans have greatly increased the concentrations of wide) bar-built estuary extending 251 km between Jupiter and nitrogen (N) and phosphorus (P) in freshwaters flowing into the Ponce inlets (Steward and VanArman, 1987; Fig. 1). Because the IRL coastal zone (Nixon, 1995; Vitousek et al., 1997; MEA, 2005), comprises a transition zone between temperate and subtropical exacerbating eutrophication and habitat loss (NRC, 2000; Bricker biomes, the IRL is considered a regional-scale ecotone and one of et al., 2007). As a result, nutrient enrichment is now a major agent the most species-diverse estuaries in North America (Swain et al., 1995). The basin includes the Mosquito Lagoon (ML) and Banana River (BR), which are located in the northern regions of the IRL. The climate of the IRL basin is humid subtropical with distinct dry and * Corresponding author. Tel.: +1 772 242 2276. E-mail address: [email protected] (B.E. Lapointe). wet seasons. Rainfall within the basin averages 140–150 cm/yr, http://dx.doi.org/10.1016/j.hal.2015.01.004 1568-9883/ß 2015 Elsevier B.V. All rights reserved. B.E. Lapointe et al. / Harmful Algae 43 (2015) 82–102 83 with 62% falling from June through October (IRLNEP, 1996). opportunities directly contributed to rapid urbanization and Freshwater enters the IRL basin from rainfall, surface water runoff, population increases. The population in the IRL region has submarine groundwater discharge (SGD), and inflows from increased from 250,000 in 1960 to 1.7 million today (US tributaries and canals. Census Bureau, 2014). As a consequence, land use changes in the The IRL watersheds have experienced dramatic changes in land- IRL watershed have been dramatic. In 1920, only 4% of the land was use over the past century. Historically, drainage of the IRL basin classified as low-density residential, while 95% of land was forest/ occurred through slow, meandering streams, creeks, rivers, and grass/pasture and 1% agriculture (Kim et al., 2002). The IRL wetlands. Since the Drainage Acts of Florida (1916) that permitted watershed is now dominated by urban land uses (39%), followed by the creation of canals to drain uplands for agriculture, reduce agriculture (24%), range (20.8%), wetland (12.1%), and natural flooding, and control mosquitos, the IRL watershed has nearly forest (4.5%; Bricker et al., 2007). tripled its size from 231,480 hectares to more than 566,560 Eutrophication of the IRL resulting from widespread urbaniza- hectares (SJRWMD, 2007). These changes greatly altered the tion and population growth has long been a concern of scientists hydrology and increased stormwater discharges to the IRL. This is and resource managers. The number of tidal inlets that allow especially evident in the St. Lucie Estuary (SLE; Fig. 1), which now flushing with Atlantic coastal waters is limited and the residence receives periodic excessive freshwater discharges from Lake time of water in the northern IRL can be high (>1 yr; Smith, 1993). Okeechobee, especially following hurricanes and tropical storms High residence times combined with rapid population growth on (Lapointe et al., 2012). Since the drainage of the IRL watersheds, its watersheds, has made the northern IRL especially susceptible to the increased land area and accompanying socio-economic nutrient enrichment, eutrophication, and seagrass die-off (Briel Fig. 1. Map of the Indian River Lagoon showing the five segments, 20 sampling sites, and four reference sites. 84 B.E. Lapointe et al. / Harmful Algae 43 (2015) 82–102 et al., 1973; Bricker et al., 2007; FDEP, 2008). Increasing land-based dolphins, Tursiops truncatus Montagu, in the IRL (Schaefer et al., sources of nutrients in surface waters of the IRL primarily originate 2009; Bossart et al., 2014). Schaefer et al. (2011) found a positive from stormwater and groundwater within agricultural and urban correlation between the number of IRL bottlenose dolphins areas on the watershed. In recent decades, urbanization of the colonized by Escherichia coli and the number of septic tanks in the watershed, especially in the northern IRL segments, has increased area they lived; with the highest number of both being in the rapidly with parallel decreases in agriculture (Duncan et al., 2004). northern segments of the IRL. Similarly, the health of juvenile In 1990, concerns of increased sewage-driven eutrophication led to green sea turtles Chelonia mydas Linnaeus as measured through the Indian River Lagoon Act of 1990 (IRL Act; Chapter 90-262, Laws blood parameters and the severity and prevalence of fibropa- of Florida) that required sewage treatment plants to cease pillomatosis (caused by an alphaherpesvirus) was significantly discharging into surface waters of the IRL by July 1, 1995. The poorer in the IRL population than those captured on adjacent IRL Act also required municipalities to identify areas where nearshore wormrock reefs (Hirama et al., 2014). package sewage treatment plants and septic tanks posed threats to Blooms of benthic macroalgae have been symptomatic of N- the IRL and implement plans to provide centralized sewage driven eutrophication in the shallow waters of the IRL for decades treatment to these areas by July 1, 1994. By 1996, point-source (Lapointe and Ryther, 1979; Benz et al., 1979; Virnstein and sewage discharges (outfalls) into surface waters of the IRL were Carbonara, 1985; Bricker et al., 2007) and provide effective largely eliminated (IRLNEP, 2008). The Watershed Restoration Act indicator organisms to assess the relative importance of N sources of 1999 (403.067 F.S.) mandated the Florida Department of and gauge the type and degree of N vs. P limitation. Macroalgae are Environmental Protection (FDEP) to scientifically evaluate the ideal ‘‘bio-observatories’’ for assessing nutrient availability as quality of Florida’s surface waters and promote the mechanisms they are typically attached to the benthos and integrate nutrient necessary to reduce nutrient pollution through the implementa- availability over temporal scales of days to weeks (Lapointe, 13 tion of the federal Total Maximum Daily Load (TMDL) program. The 1985). Measurement of stable carbon and nitrogen isotopes (d C, 15 effort of the implementation was mainly geared toward the d N) in macroalgal tissue have been widely used to discriminate reduction of nutrient inputs from wastewater treatment plants among natural (upwelling, N-fixation) and anthropogenic (sew- (WWTPs) and stormwater runoff.