Ecosystem responses to long-term nutrient management in an urban estuary: Tampa Bay, Florida, USA

Estuarine, Coastal and Shelf Science xxx (2014) 1e16

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Invited feature

Ecosystem responses to long-term nutrient management in an urban estuary: Tampa Bay, Florida, USA H. Greening a, *, A. Janicki b, E.T. Sherwood a, R. Pribble b, J.O.R. Johansson b a b

Tampa Bay Estuary Program, 263 13th Ave S., Suite 350, St. Petersburg, FL 33701, USA Janicki Environmental, Inc., 1155 Eden Isle Drive NE, St. Petersburg, FL 33704, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Accepted 7 October 2014 Available online xxx

In subtropical Tampa Bay, Florida, USA, we evaluated restoration trajectories before and after nutrient management strategies were implemented using long-term trends in nutrient loading, water quality, primary production, and seagrass extent. Following citizen demands for action, reduction in wastewater nutrient loading of approximately 90% in the late 1970s lowered external total nitrogen (TN) loading by more than 50% within three years. Continuing nutrient management actions from public and private sectors were associated with a steadily declining TN load rate and with concomitant reduction in chlorophyll-a concentrations and ambient nutrient concentrations since the mid-1980s, despite an increase of more than 1 M people living within the Tampa Bay metropolitan area. Water quality (chlorophyll-a concentration, water clarity as indicated by Secchi disk depth, total nitrogen concentration and dissolved oxygen) and seagrass coverage are approaching conditions observed in the 1950s, before the large increases in human population in the watershed. Following recovery from an extreme weather event in 1997e1998, water clarity increased significantly and seagrass is expanding at a rate significantly different than before the event, suggesting a feedback mechanism as observed in other systems. Key elements supporting the nutrient management strategy and concomitant ecosystem recovery in Tampa Bay include: 1) active community involvement, including agreement about quantifiable restoration goals; 2) regulatory and voluntary reduction in nutrient loadings from point, atmospheric, and nonpoint sources; 3) long-term water quality and seagrass extent monitoring; and 4) a commitment from public and private sectors to work together to attain restoration goals. A shift from a turbid, phytoplanktonbased system to a clear water, seagrass-based system that began in the 1980s following comprehensive nutrient loading reductions has resulted in a present-day Tampa Bay which looks and functions much like it did in the relatively pre-disturbance 1950s period. © 2014 Elsevier Ltd. All rights reserved.

Keywords: ecosystem recovery eutrophication watershed management seagrass USA Florida Tampa Bay

1. Introduction A primary water quality challenge facing estuaries throughout the world is cultural eutrophication e a process in which human activities in the watershed and airshed lead to increased nutrient influxes to the water body, producing levels of over-fertilization that stimulate undesirable blooms of phytoplankton and macroalgae (Nixon, 1995; Bricker et al., 1999, 2007; NRC, 2000; Cloern, 2001; Duarte et al., 2013). Such blooms affect estuarine ecosystems in several ways. They reduce water clarity and block sunlight, reducing the size, quality, and viability of submerged aquatic vegetation (SAV) including seagrass meadows and other aquatic

* Corresponding author. E-mail address: [email protected] (H. Greening).

habitats. Several bloom-forming phytoplankton species also produce toxins that can negatively affect the structure and function of aquatic food webs (Anderson et al., 2002) and pose health threats to wildlife and humans (Burns, 2008). As phytoplankton and macroalgae die and decompose, dissolved oxygen (DO) is removed from the water column and bottom sediments. Because an adequate supply of DO is essential to the survival of most aquatic organisms, such reductions can have substantial impacts on the local fauna (Gray et al., 2002; Diaz and Rosenberg, 2008). Eutrophic conditions are widespreaddin 1999, Bricker et al. concluded that nearly all estuarine waters in the USA now exhibit some symptoms of eutrophication. Cases of gradual estuarine eutrophication have been known for more than 50 years and include large systems such as Chesapeake Bay (Boesch et al., 2001; Kemp et al., 2005; Williams et al., 2010) and the Baltic Sea (Osterblom et al., 2007; Helsinki Commission, 2009), and smaller systems such as Waquoit Bay,

http://dx.doi.org/10.1016/j.ecss.2014.10.003 0272-7714/© 2014 Elsevier Ltd. All rights reserved.

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Massachusetts (Valiela et al., 1992; Valiela and Bartholomew, 2014). Several recent examples demonstrate rapid eutrophication after years of recovery. In the Indian River Lagoon, Florida, USA, nutrient loading decreased and seagrass exhibited a gradual increase from 1980s through 2010 (St. Johns River Water Management District, 2012). Extreme cold weather in 2011 was followed by a ‘superbloom’ of microalgae. This severe freeze resulted in a significant die-back of macroalgae that in turn increased nutrient concentrations and the eventual bloom. With the microalgal bloom, light attenuation increased to the point where a dramatic seagrass decline of 60% coverage was observed during four years. In Maryland/Virginia coastal bays, USA, observed water quality conditions improved between 1992 (when records began) and the late 1990s, but has been declining since then as a result of steadily increasing anthropogenic nutrient inputs (Glibert et al., 2013). Examples of recovery from eutrophic conditions also exist, but are much more uncommon. Duarte et al. (2013) examined definitions of estuarine and coastal ecosystem recovery in published examples, and found that partial (as opposed to full) recovery prevailed; that degradation and recovery typically followed different pathways; and that recovery trajectories depended on the nature of the pressure as well as the connectivity of an ecosystem. They found a few examples of successful ecosystem recovery to date, including eelgrass recovery in Virginia coastal bays (Orth and McGlathery, 2012); water quality and seagrass recovery in Tampa Bay, Florida (Greening et al., 2011) and single species recovery (Jones and Schmitz, 2009). Other examples of estuarine-scale ecosystem recovery in response to significant decreases in nutrient loading include Kaneohe Bay, Hawaii; Boston Harbor, Massachusetts; and areas of Chesapeake Bay. Kaneohe Bay received increasing amounts of wastewater from the 1950s through 1977, at which time most of the wastewater was diverted from the bay. Following the diversion, the biomass of both plankton and benthos decreased rapidly, while the benthic biological community had not returned to pre-discharge conditions by 1980 (Smith et al., 1981). In Boston Harbor, Massachusetts, significant water quality improvements were observed as a result of the installation of the Deer Island advanced tertiary wastewater treatment facility and outfall pipe from 1991 to 2000. Loadings of total nitrogen, total phosphorus, and particulate organic carbon decreased between ~80% and ~90% (Taylor et al., 2011), and five years after the outfall went online, water quality met current thresholds for eelgrass requirements (Taylor, 2006; Leschen et al., 2010). Similarly, sharp reductions in a wastewater nutrient loading rate resulted in improved water quality and increased SAV coverage and density after initial lag times in Mattawoman Creek, Maryland (Boynton et al., 2014). In other areas of the Chesapeake Bay, a resurgence of SAV has also been attributed to nutrient load reductions from wastewater treatment facilities (Kemp et al., 2005; Orth et al., 2010). Chainho et al. (2010) observed significant positive metrics for benthic communities following reduced nutrient loads from wastewater treatment facilities in the Tagus Estuary, Portugal. There are numerous examples of how estuarine systems respond to increased nutrient loading and eutrophication over time, but fewer examples of the reverse. In this paper, we evaluate the restoration trajectory of a subtropical urban estuarine system recovering from severe eutrophication symptoms (Tampa Bay, Florida, USA). Following a characterization of present-day Tampa Bay, we define historic degradation of the ecosystem, key management decisions and actions taken by the Tampa Bay community, and ecosystem responses to resulting nutrient reductions. Contrary to many other estuaries worldwide, Tampa Bay appears to be recovering to relatively pre-disturbance conditions as a result of continuing implementation of the nutrient management strategy

defined by the community. We examine the patterns of recovery relative to current paradigms of regime shifts and restoration trajectories, and identify key science, management, and policy elements critical to the continuation of Tampa Bay's recovery. The Tampa Bay technical, academic and resource management community has been involved for more than 25 years in development of the scientific basis for quantifying restoration and protection targets; evaluating management options; and tracking responses in the Bay's condition. This process is documented in a series of Technical Publications listed in the Supplemental Information. 2. Tampa Bay characteristics Tampa Bay is a large (water surface area of 1036 km2), shallow (mean depth 4 m), Y-shaped embayment located on the westcentral coast of the Florida peninsula, USA (Fig. 1). The bay is Florida's largest open-water estuary, and receives fresh water runoff from a watershed that covers an area of about 5700 km2. Its bathymetry has been modified by the construction and maintenance of an extensive network of shipping channels, dredged to depths of about 13 m. Model-based estimates of bay-wide residence times range from weeks to months and are primarily influenced by tides, winds, and the historic dredging alterations to bathymetry (Weisberg and Zheng, 2006; Meyers et al., 2013). Because of its relatively large size, the gradient of freshwater to saltwater habitats it provides, and its location in a transition zone between warm-temperate and tropical biogeographic provinces, the bay and its contributing watershed support a highly diverse flora and fauna and represent a regionally significant environmental resource (Lewis and Estevez, 1988; Wolfe and Drew, 1990; Yates et al., 2011). Tampa Bay's four major segments differ both in terms of their physical setting and their contributing watersheds (Table 1). Hillsborough Bay, occupying the northeastern portion of Tampa Bay, is the smallest in terms of surface area and volume but has a large watershed, thereby having the lowest bay surface area to watershed area ratio. Hillsborough Bay receives much of its freshwater inputs via the Hillsborough River, Alafia River, and the Tampa Bypass Canal. It also receives the bulk of the point sources loads to Tampa Bay, particularly from the City of Tampa's advanced wastewater treatment plant. As a result, nutrient loading to Hillsborough Bay is larger than any other bay segment. Circulation in Hillsborough Bay is largely influenced by these inputs as well as a significant shipping channel that extends from the Port of Tampa to the Gulf of Mexico. Old Tampa Bay, located in the northwestern portion of Tampa Bay, in contrast to Hillsborough Bay, is characterized by a relatively high bay surface area to watershed area. Old Tampa Bay is most notable for the three causeway/bridge structures that influence its hydrodynamics. Circulation studies have shown that waters leaving Hillsborough Bay often find their way into Old Tampa Bay (Meyers et al., 2013). Middle Tampa Bay is the largest segment in terms of area, and has a relatively large volume. Much of the water entering Middle Tampa Bay is transported from both Hillsborough Bay and Old Tampa Bay. There is considerable exchange of water from this bay segment with Lower Tampa Bay as well. The Little Manatee River is the major freshwater source to Middle Tampa Bay. Lower Tampa Bay is the largest of the bay segments in terms of volume. Significant tidal exchange with the Gulf of Mexico and Middle Tampa Bay are the major influences on the hydrodynamics of Lower Tampa Bay. The Manatee River drains into Lower Tampa Bay and is its largest freshwater input. Much of the land area that adjoins the bay is highly urbanized, including the cities of Tampa, St. Petersburg, Clearwater, and

Please cite this article in press as: Greening, H., et al., Ecosystem responses to long-term nutrient management in an urban estuary: Tampa Bay, Florida, USA, Estuarine, Coastal and Shelf Science (2014), http://dx.doi.org/10.1016/j.ecss.2014.10.003

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Fig. 1. Tampa Bay location and 2010 land use map of the watershed. Source: Southwest Florida Water Management District (SWFWMD).

Bradenton, as well as numerous smaller municipalities (Fig. 1). More than two million people currently live within the three counties that directly border the bay, a number that has more than quadrupled since the early 1950s (Yates et al., 2011). The population of the seven-county Tampa Bay region (portions of which lie outside the watershed), which was about 3.5 million in 2000, has been projected to increase to seven million by the year 2050 (Urban Land Institute Tampa Bay District Council, 2008). The bay shoreline is dominated by urban land uses on its northern and western sides and by a combination of agricultural, industrial, and rapidly increasing suburban land uses on the east, while much of the southern extent is natural shoreline. Several active port facilities with bulk commercial shipping interests occur in the upper

and lower bay and are an important component of the local economy. The Tampa Bay drainage basin differs from many other estuaries because extensive phosphate deposits are actively mined for fertilizer production in its watershed. Large amounts of phosphorus ore and processed fertilizer products are shipped world-wide from Tampa Bay terminals. Natural leaching of these deposits and the mining activities are considered responsible for the substantial and established phosphate enrichment of Tampa Bay estuarine waters. Fanning and Bell (1985) summarized the uniqueness of Tampa Bay among other estuaries in terms of phosphorus enrichment as: “Compared to other estuaries and coastal waters, Tampa Bay is considerably enriched in phosphate. In fact, no other major

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Table 1 Characteristics of the four major bay segments in Tampa Bay. Bay segment

Surface area (km2)

Volume (million m3)

Average depth (m)

Watershed area (km2)

Lower Tampa Bay Middle Tampa Bay Old Tampa Bay Hillsborough Bay

247 310 200 105

1200 1166 548 306

4 4 3 3

298 952 774 2797

estuarine or coastal area we know of even comes close to having as high a phosphate concentration.” The uniquely high ambient phosphorus concentrations of Tampa Bay waters result in an unusually low nitrogen to phosphorus ratio in comparison to other estuaries. Generally, the Tampa Bay N:P ratio is substantially below the molar ratio of 16, which is considered an upper threshold for nitrogen deficiency, thus suggesting that the Tampa Bay phytoplankton population is strongly nitrogen limited (Greening and Janicki, 2006). Numerous nutrient limitation studies using natural Tampa Bay phytoplankton populations and cultured test organisms have confirmed nitrogen limitation. The studies have concluded that the availability of nitrogen generally is the primary limiting nutrient for phytoplankton growth in the estuarine waters of Tampa Bay (Vargo et al., 1994; Johansson, 2009). Specifically, the most recent referenced study conducted 152 nutrient bioassay tests on natural phytoplankton populations in the four main stem segments of Tampa Bay from 1993 to 2009; of those, 149 indicated that nitrogen was the stronger limiting nutrient. None of the tests indicated that phosphorus was the stronger limiting nutrient. Although in situ nutrient concentrations for both N and P within Tampa Bay may be considered sufficient for algal growth regardless of N:P ratios, chlorophyll-a variation in the bay responds most significantly to

Fig. 3. Population in the three counties surrounding Tampa Bay, 1940e2010 (US Census Bureau). Projected population in the three counties in 2050 (Urban Land Institute Tampa Bay District Council, 2008).

watershed TN loads (Greening and Janicki, 2006). Thus, precluding additional TN loads to the bay has been the primary focus for managing nutrients entering Tampa Bay. 3. Tampa Bay e historical loss and stage for recovery In the late 1970s and 1980s, the degrading ecological condition of Tampa Bay became more visible to its surrounding human community. Macroalgae were washing up on shorelines (e.g., Fig. 2

Fig. 2. Comparison of current aerial photography (2011) showing patchy seagrass (Halodule wrightii) beds relative to the same area in Tampa Bay covered by Ulva spp. mats circa 1980s. Photo courtesy of J.O.R. Johansson; aerial photo courtesy of SWFWMD.

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insert), noxious phytoplankton blooms were occurring, seagrass beds were disappearing, marsh habitats were being filled as a result of rapid coastal development, and populations of valued macrofauna such as birds, fish, and manatees were decreasing (Yates et al., 2011; Morrison et al., 2014). These observations coincided with a rapid increase in population, from less than 0.5 M in 1950 to 1.5 M in 1980 (Fig. 3). In Tampa Bay, symptoms of cultural eutrophication became pronounced during the 1970s and early 1980s, a period when the bay was receiving much larger nutrient inputs than it does today. The symptoms included large and frequent blooms of phytoplankton and macroalgae, reduced water clarity, reductions in the condition and areal extent of seagrass beds, increased variability in dissolved oxygen concentrations, and more frequent episodes of stressfully-low (hypoxic to anoxic) dissolved oxygen levels. Eutrophication impacts were particularly severe in Hillsborough Bay, the portion of Tampa Bay that was receiving the largest inputs of municipal sewage effluent and industrial leaks and spills during that period (Santos and Simon, 1980; Johansson and Lewis, 1992).

4. Regional management response e A call to action Several key events have occurred within the Tampa Bay region which influenced the bay's recovery (Table 2). Beginning in the late 1970s and continuing throughout the present recovery period, considerable citizen input and pressure shaped the management efforts of both public and private entities and stakeholders. A major turning point for Tampa Bay occurred in the 1980s when implementation of state legislation known as the Grizzle-Figg Act (Florida Statute 403.086) came into effect requiring more stringent treatment standards for wastewater plants discharging to Tampa Bay and its watershed. This legislation was prompted by citizen demands to local and state officials to improve the water quality of Tampa Bay. Upgrades to the City of Tampa's Howard F. Curren Plant during the late 1970s to advanced wastewater treatment increased nutrient removal and significantly reduced the amount of nitrogen being discharged directly into the bay. Also, the City of St. Petersburg pioneered the country's first large-scale reclaimed wastewater program, reusing treated wastewater for irrigation of lawns and golf courses rather than discharging it directly into the bay. The advanced treatment and reuse standards set forth in Grizzle-Figg legislation provided the bay with a kick start for its turnaround. Nonpoint nutrient sources have also been addressed through regulation. In 1985, FDEP enacted statewide permitting requirements for non-agricultural stormwater systems, reducing nutrient and sediment loading from urban and residential stormwater. Continuing citizen-led efforts during the 1980s through present have resulted in regional and collaborative visions for restoring Tampa Bay that have been implemented through several Table 2 Timeline of management events that have coincided with Tampa Bay's recovery. Date

Milestone

1980

Grizzle-Figg Act requiring TN reductions from wastewater treatment plants implemented Stormwater permitting implemented Tampa Bay Estuary Program established Tampa Bay Nitrogen Management Consortium (TBNMC) formed FDEP accepts TBNMC Action Plan as meeting regulatory requirements Power plant repowerings begin FDEP accepts TBNMC recommendations of TN loading allocations to individual sources Tampa Bay Estuary Numeric Nutrient Criteria recommendations enacted by the State

1985 1991 1996 2002 2004 2010 2012

5

governmental entities, including the Tampa Bay Regional Planning Council's Agency on Bay Management and the Tampa Bay Estuary Program (TBEP). The TBEP was established in 1991 to help local governments, agencies, and other stakeholders in the Tampa Bay area develop a plan to sustain the recovery of Tampa Bay. The TBEP partners adopted a Comprehensive Conservation and Management Plan in December 1996 (subsequently updated in 2006; TBEP, 2006) that included measurable goals for the achievement of the Bay's designated uses and to support full aquatic life protection. Among these goals was the restoration of bay water quality to support the recovery of seagrass resources while maintaining and enhancing the Bay's fisheries production and other designated uses. Significant resources, commitments, and investments have been made by TBEP partners to achieve this goal. Public and private parties that comprise the TBEP management and policy boards unanimously adopted a strategy that established targets that maintained nutrient loading to the major bay segments of Tampa Bay to commensurate levels estimated from the 1992e1994 period. The targets ensure that adequate water clarity and light levels are maintained in the bay on an annual basis to promote seagrass recovery. These targets also provide a balance between the recovery of seagrass resources and maintaining and enhancing the phytoplankton-based food web and fisheries production long recognized in Tampa Bay. To further reinforce their commitment in maintaining these ecosystem-based restoration goals for Tampa Bay, local government and agency partners formally adopted an Interlocal Agreement in 1998. Also in 1996, TBEP's governmental partners joined with key industries in the Tampa Bay region to create an ad-hoc public/private partnership known as the Tampa Bay Nitrogen Management Consortium (TBNMC). The TBNMC's objective was to implement an Action Plan to meet the protective nutrient load targets developed for Tampa Bay. The original Consortium Action Plan, entitled Partnership for Progress, consisted of more than 100 projects that collectively reduced or precluded nitrogen discharges to the bay by more than 224,000 kg each year (or about 5% of the total Tampa Bay load) between 1995 and 1999. Since 1999, additional projects have been implemented to reduce nitrogen loads to the bay by about 270,000 kg each year (or about 7.9% of the average total Tampa Bay load from 2000 to 2011). In total, from 1992 to 2013, TBNMC participants have invested over $430 M in projects and actions to reduce nutrient loads to Tampa Bay in order to voluntarily meet the protective load targets for the bay. The management of nutrient loadings to Tampa Bay included actions to reduce atmospheric deposition and nonpoint source loadings related to agricultural and mining activities. In 1999, the Tampa Electric Company reached agreement with the U.S. Environmental Protection Agency (EPA) and the Florida Department of Environmental Protection (FDEP) to dramatically reduce overall emissions from Tampa Electric Company's power plants. Its Selective Catalytic Reduction project addressed the nitrogen oxide emissions as did the repowering of the coal-burning Gannon Power Station to natural gas in 2004. Other electric power generating plants located within the Tampa Bay watershed are also in the process of repowering from coal or oil to natural gas. The completion of these efforts is expected to result in the annual reduction of NOx emissions from electric power plants by 90% (Poor et al. 2012). To address the influence of agricultural practices on nutrient loading to Tampa Bay, the Florida Department of Agriculture and Community Services has been working with stakeholders to develop Best Management Practices (BMPs) specific to their agricultural practices (http://www.freshfromflorida.com/DivisionsOffices/Agricultural-Water-Policy/). The influence of phosphate mining on Tampa Bay nutrient loadings are regulated by the

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National Pollutant Discharge Elimination System (NPDES). The NPDES permitting process in combination with significant reductions in water use by the mining industry has also led to improvement in nutrient loading to Tampa Bay. In 1998, the EPA recognized a regulatory Total Maximum Daily Load (TMDL) for Tampa Bay, based on management targets set by TBEP to support recovery of seagrass. Tampa Bay Nitrogen Management Consortium participants, in coordination with EPA and FDEP, agreed to develop voluntary nitrogen limits for themselves and provide those limits as recommendations, rather than relying on the regulatory agencies to develop allocated numeric limits. Over a two-year period, TBNMC members developed fair and equitable allocations for all 189 sources within the watershed, resulting in a TN discharge cap on each load source at levels observed in 1992e1994. The FDEP and EPA accepted those recommended allocations as meeting requirements for the TMDL. In addition, in November 2002 and subsequently in 2007 and 2012, FDEP concluded that the TBNMC's nitrogen management strategy provided reasonable assurance that the state water quality criteria for nutrients would be met in Tampa Bay. Both FDEP's reasonable assurance determination and the total maximum nitrogen loading recognized by EPA are based on statistical modeling and data analyses peer-reviewed by the TBEP, its partners, and state and federal regulators. The TN loading targets that were established for Tampa Bay were eventually also used to define numeric nutrient criteria (NNC). Both EPA and FDEP reviewed the target setting process and adopted the TN loading targets as NNC for Tampa Bay. In addition, the chlorophyll-a concentration and seagrass targets were adopted by these regulatory agencies as part of an overall water quality improvement program. Thus, the TBNMC's voluntary nutrient loading targets developed for the major bay segments of Tampa Bay have been acknowledged by both state and federal regulators as protective nutrient loads for this estuary. More recently, several local governments in the Tampa Bay watershed have enacted residential fertilizer ordinances, restricting the use of nitrogen and phosphorus fertilizer in the summer rainy season. The successful nutrient management strategy that has evolved from the efforts of local governments, agencies, and industry participants of the TBNMC since the 1990s has further influenced the Bay's recovery during the past 20 years. 4.1. Establishment of targets for Tampa Bay's recovery Early on in the process, Tampa Bay's management partnership developed numerical seagrass protection and restoration goals, and has adopted numerical water transparency targets (expressed as annual mean Secchi disk depths), chlorophyll-a concentrations, and TN loading rates in order to meet those goals. The development of the goals and targets followed a multi-step process (Greening and Janicki, 2006; Greening et al., 2011) that involved joint collaboration between public and private sectors. 4.1.1. Step 1. set specific, quantitative seagrass coverage goals for each bay segment In 1996, the local management community adopted a minimum seagrass coverage goal of 15,380 ha, which represents 95% of the areal coverage that was estimated to have been present in the bay in the early 1950s (after subtracting areas that have been rendered non-restorable by subsequent dredging, filling and the construction of causeways and other infrastructure). The early-1950s time period was selected as the baseline for seagrass coverage because it preceded the rapid population increases that have occurred in the watershed in more recent decades, and because aerial photographs

from the period were available for the entire Tampa Bay shoreline and adjacent shallow water (Greening and Janicki, 2006). 4.1.2. Step 2. determine the light requirements of the primary target seagrass species (Thalassia testudinum) in Tampa Bay Field studies carried out in stable T. testudinum meadows in Lower Tampa Bay indicated that the deep edges of those beds corresponded to the depth at which 20.5% of Io (the light that penetrates the water surface) reached the bottom on an annual average basis (Dixon, 1999). 4.1.3. Step 3: determine the water clarity levels necessary to provide adequate light to meet the seagrass acreage goals Based on the 20.5% light requirement estimated in Step 2, the seagrass acreage restoration goal was restated as a light penetration and water clarity target: to restore seagrass cover to early-1950s levels in a given bay segment, water clarity in that segment should be restored to a point that allows at least 20.5% of Io to reach the same depths that were mapped in the early 1950s. Those depths range from 1.0 m for Hillsborough Bay to 2.0 m for Lower Tampa Bay (Greening and Janicki, 2006). 4.1.4. Step 4: determine maximum chlorophyll-a concentrations that allow water clarity to be maintained at appropriate levels Water clarity and light penetration in Tampa Bay are affected by a number of factors, including phytoplankton density (estimated using measured chlorophyll-a concentrations), colored dissolved organic material (CDOM, estimated using water color measurements), and non-phytoplankton turbidity (McPherson and Miller, 1994). Regression analyses applied to the long-term monitoring data collected by the Environmental Protection Commission of Hillsborough County (EPCHC) during the 1974e1994 period to were used to develop an empirical model describing water clarity variations in response to these factors in the four largest bay segments. The model that provided the best fit (highest R2) to the observed water clarity data took the form:

ln Ct;s ¼ at;s þ bt;s *ln Zt;s




where Zt,s is the depth to which 20.5% of surface irradiance penetrates in month t and bay segment s; Ct,s is the average chlorophylla concentration in month t and bay segment s; and at,s and bt,s are regression parameters (Greening and Janicki, 2006). Least-squares regression methods were used to estimate the regression parameters. Results of the regressions indicated that variation in observed depths to which 20.5% of surface irradiance penetrates could be explained by variations in observed chlorophyll-a concentration. Monthly specific regression intercept terms were used to avoid any potentially confounding effects of seasonality in independent and dependent variables. The model fit was relatively good (R2 ¼ 0.67). Turbidity and water color were also investigated as possible explanatory variables, but provided no significant improvements in model fit. The segment-specific annual average chlorophyll-a concentration targets developed using this process, which range from 4.6 mg/ L to 13.2 mg/L in the four major bay segments, can be tracked through time and used as an annual indicator to assess success in maintaining water quality requirements necessary to meet the long-term seagrass coverage goal (Greening and Janicki, 2006). 4.1.5. Step 5: determine maximum nutrient loadings that allow chlorophyll-a concentration targets to be achieved Examination of the available water quality monitoring data during the mid-1990s indicated that the water clarity conditions that existed during the years 1992 through 1994 allowed an annual

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average of more than 20.5% of subsurface irradiance (Io) to reach target depths (the estimated depths to which seagrasses grew in the early 1950s) in three of the four largest bay segments. A nitrogen load management strategy based on ‘holding the line’ at the annual loading levels estimated to have occurred during the 1992e1994 period was therefore adopted by the TBEP and its partners (Greening and Janicki, 2006). For consistency with the adaptive management approach, the effectiveness of the ‘hold the line’ nitrogen management strategy is assessed annually, by evaluating chlorophyll-a concentrations and water clarity levels measured by the local monitoring programs in each bay segment during the previous calendar year, and comparing those values to the segment-specific targets (Greening and Janicki, 2006). 5. Ecosystem responses to management 5.1. Nutrient loadings A series of projects have been carried out to estimate the sources, magnitudes, and pathways of both new and recycled N and their effects on bay water quality. Monthly loadings to Tampa Bay have been estimated for the period 1985 through 2011. TN loadings to Tampa Bay are from seven different source categories, including atmospheric deposition directly to the surface of the bay, domestic and industrial point sources, material losses from fertilizer handling facilities, springs, groundwater inflows around the shore of the bay, and nonpoint source runoff. Atmospheric deposition directly to the surface of the bay is defined as the sum of wet deposition (rainfall) and dry deposition (gaseous constituent interaction and dust fallout). Estimates of rainfall are derived from a set of National Weather Service stations around Tampa Bay. Estimates of nitrogen concentrations in rainfall are derived from data collected at the National Atmospheric Deposition Program Verna Wellfield site and at the near-bay site monitored as part of the Tampa Bay Atmospheric Deposition Study (TBADS) during 1996e2006 (Poor et al., 2012). As part of the TBADS, dry deposition rates were estimated as well, and the wet:dry deposition ratio developed that was applied to estimate total atmospheric deposition (AD) rates. Atmospheric deposition to the watershed was included in the nonpoint source category. Domestic wastewater treatment facilities discharge to the Tampa Bay watershed and directly to the bay. Data are collected from FDEP for each of the 33 facilities discharging to the watershed or bay which have annual average daily discharges of 0.1 million gallons per day (MGD) or greater. Monthly discharge volume and nutrient concentrations are utilized to develop loadings from these facilities. Loadings from both surface water discharges and discharges for irrigation are estimated as domestic point sources (DPS). Based on United States Geological Survey (USGS) studies in the Tampa Bay watershed, 5e10% of TN applied to the watershed as reclaimed wastewater is estimated to reach Tampa Bay (Reichenbaugh et al., 1979). Although small pockets of the urbanized areas in the Tampa Bay watershed remain on individual septic systems, the majority is served by central sewer (Tampa Bay Water Atlas; http://www. tampabay.wateratlas.usf.edu/new/). Less densely populated and rural areas outside of the urban service areas in the eastern part of the watershed are also served by individual septic systems and some small package plants. Industrial point sources (IPS) include discharges of process water and other effluent not categorized as domestic sewage. As for domestic wastewater facilities, data are collected from FDEP for each of the 39 facilities discharging to the watershed or bay which have annual average daily discharges of 0.1 MGD or greater. Monthly data are used to develop loadings from these facilities.

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Many of these facilities are associated with phosphate mining activities in the watershed. Phosphate mining in the Tampa Bay watershed contributes to its uniqueness. Port Tampa Bay and Port Manatee facilities are used to ship fertilizer product, and the fertilizer handling operations (storage, ship loading, and product transfer) result in some loss of product directly to the bay. Estimations of these losses were developed in consultation with the port authorities and the fertilizer companies. Groundwater inputs along the shoreline also contribute nitrogen to the bay. These loadings are estimated relatively grossly utilizing USGS potentiometric surface maps and observed groundwater quality data. The surficial (water table), intermediate, and Floridan aquifers all contribute flows and loads to Tampa Bay. Observed groundwater quality data and potentiometric surfaces are combined with aquifer transmissivity taken from local groundwater modeling efforts, and flow length paths, to derived nutrient loadings from groundwater (GW). Three relatively large springs discharge to tributaries of Hillsborough Bay, and loading estimates are derived from measured flow and water quality data. Finally, nonpoint source (NPS) pollutant loadings result from stormwater runoff to the bay and base flow from the rivers to the bay, and include atmospheric deposition deposited on the watershed. Loadings are estimated utilizing observed flow and water quality data for those regions of the watershed where these data are available. In those portions of the watershed where flow data are lacking (about one-third of the watershed), an empirical model developed from observed Tampa Bay watershed flow data is used to estimate flows, utilizing observed rainfall data, land use, and soils. The model estimates monthly flows as a function of both the samemonth rainfall and the rainfall during the two preceding months. Similarly, in those portions of the watershed without water quality monitoring data available, land use is utilized to estimate pollutant concentrations for derivation of loadings, based on land usespecific concentrations (Greening and Janicki, 2006). The major nonpoint sources in the Tampa Bay watershed, other than typical urban sources, include a variety of agricultural land uses and phosphate mining (Greening and Janicki, 2006). Given its semi-tropical climate, the Tampa Bay watershed is notable for citrus groves as well as a series of row crops that require fertilization and irrigation. Rangelands represent the largest contribution to the total agricultural land uses.

Fig. 4. Estimated annual loads of total nitrogen from various sources to Tampa Bay summarized from 1976 to 2011 (from Greening and Janicki, 2006).

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On a baywide basis, there were marked responses in the environment to the management and regulatory actions taken since the early 1980s. Most notable was the reduction in TN load from point sources (PS). Decadal trends show that point source TN loads declined from a ca. 1976 worst case load of 5.4 million kg/yr to 0.5 million kg/yr by the mid-1980s (Fig. 4). This translated to a reduction in PS percent contributions from 60% relative to the 9 million kg/yr total load in ca. 1976 to 20% of the 3.5 million kg/yr total load in 2000e2011 (Table 3). Similar results were obtained for TP loadings to Tampa Bay (Greening and Janicki, 2006). Nonpoint sources have now become the predominant TN load to Tampa Bay, contributing >57% of the total external nutrient load to the bay. The contribution of atmospheric deposition nitrogen loading directly to the bay's surface in the early 1990s was estimated to be approximately 25e30% of the total TN loading to Tampa Bay (Greening and Janicki, 2006). Recognizing the importance of this loading source, a series of projects (the Bay Regional Atmospheric Chemistry Experiment or BRACE) was undertaken to better understand the role of this source in the attempts to restore Tampa Bay water quality (Poor et al., 2012). The BRACE program provided an improved estimate of atmospheric reactive nitrogen (N) deposition to Tampa Bay, apportioned atmospheric N between local and remote sources, and assessed the impact of regulatory drivers on N deposition. They found that oxidized N emissions from mobile sources had a disproportionately larger impact than did power plant sources on atmospheric N loading. Predicted decreases in atmospheric N deposition to Tampa Bay by 2010 due to regulatory drivers were significant, and evident in recent declines in ambient air NOx concentrations in urban Tampa and St. Petersburg (Poor et al., 2012). When considering the population of Tampa Bay from the 1970s to 2011 (Fig. 3), TN load per capita continues to decrease. In the 1970s, per capita TN load was approximately 6.6 kg/person/yr. From 1985 to 1989 it was approximately 2.1 kg/person/yr; from 1990 to 1999, 1.8 kg/person/yr; and from 2000 to 2011, 1.3 kg/person/yr. These continued declines reflect an ever expanding populace, but with reduced and declining TN loads entering the bay from the watershed, due to implementation of multiple nutrient reduction projects and programs outlined in Section 4. Further translated, current per capita TN load has declined by about 80% since the early 1980s. In summary, three significant responses in nutrient loadings to the management and regulatory actions occurred in Tampa Bay: 1) reduced overall TN loading to Tampa Bay; 2) reduced TN loads per capita, and 3) a change in the nature of the TN loads from one dominated by point sources to one dominated by nonpoint sources (Fig. 4). 5.2. Bay water quality and clarity Both TN and TP concentrations in each of the four major bay segments declined significantly following nutrient loading reductions (Fig. 5a, b). These reductions have resulted in TN and TP Table 3 Relative contributions of the various sources of nitrogen loads to Tampa Bay in the 1970s and the 2000s. Adapted from Greening and Janicki (2006). Source

1970s Contribution (%)

2000e2011 Contribution (%)

Point sources Nonpoint sources Atmospheric deposition Fertilizer handling losses Groundwater & Springs

60.3 23.9 10.8 4.9 0.1

19.5 57.4 20.4 0.5 2.1

Total

100 (8,984,760 kg)

100 (3,410,582 kg)

concentrations that have been consistently lower by at least 50% ~ o heavy rainfall period. The observed trends since a 1998 El Nin were examined using the Seasonal Kendall Tau method on mean monthly data during the 1974e2013 period. Both TN and TP concentrations showed significant declining trends during this period (P < 0.0001, respectively). In addition, recent observations in all bay segments remain below guidance target values established by TBEP for the protection of seagrass resources in the bay. The continuing decline in TN and TP concentrations, even as nutrient loads have remained relatively constant following sharp declines between 1976 and 1985 (Fig. 4), may be due to a reduction in the rate of release of nutrients to the water column from the sediments over time. During periods of high external nutrient loading, others have observed increased sediment nutrient concentrations in lakes (Hou et al., 2013) and seasonally in coastal waters (Rozan et al., 2002). Fillos and Swanson (1975) found that biogeochemical processes may result in gradual release of accumulated nutrients in the sediment sufficient to maintain the eutrophic state of overlying water long after external sources have been eliminated. In Tampa Bay, internal cycling of nitrogen provides a significant source of nutrients for ecosystem production. Use of a mechanistic water quality model for the period 1985e1994 Wang et al. (1999) indicated that the internal recycling and regeneration processes strongly impacted water column nitrogen concentrations. Given the results of the modeling effort, it was expected that external load reductions may well not immediately result in detectable improvements in water quality. However, it was surmised that longer-term sustained reductions would lead to reduced internal nutrient pools available for recycling and regeneration. Reductions in chlorophyll-a concentration were also observed over the period of record (Fig. 6). The largest reduction was seen in Hillsborough Bay which has historically received the greatest PS loadings in addition to the majority of freshwater inputs to Tampa Bay. In all four segments, current chlorophyll-a concentrations have been consistently lower than historic periods with a few exceptions related to above-average rainfall conditions (e.g., 1994 and 1998 El ~ o years), and to occasional summer nuisance algae blooms Nin (Pyrodinium bahamense) in upper Old Tampa Bay (2009 and 2011). The blooms resulted in water discoloration and reduced clarity during summer months and excessive chlorophyll-a concentrations during these months in the Old Tampa Bay segment; however, fish kills and human-health impacts were not reported. Similar to that observed for TN and TP concentrations, observed lags between the major load reductions to Tampa Bay and the corresponding response in water column chlorophyll-a concentration have been suggested as the time needed for internal processes to respond to reduced nitrogen loading (Johansson, 1991). The results of the Wang et al. (1999) effort indicated that the total mass of nitrogen in the bay decreased during the 1985e1994 period. Relationships in chlorophyll-a concentrations, nutrient loadings, and nutrient concentrations have been previously examined through development of the nutrient management strategy for Tampa Bay (Greening and Janicki, 2006). Because there was little relationship between inebay TN concentrations and antecedent TN loading from the watershed, the Tampa Bay resource management community concluded that managing TN loads, rather than inebay concentrations would most successfully achieve the Bay's recovery goals. Further, for the period 1985e1994, a simple empirical relationship between monthly mean chlorophyll-a concentrations and cumulative, 3-month TN loading to each of the 4 major bay segments (R2 ¼ 0.69) was the most robust predictor for bay management purposes. The empirical model was updated for the 1985e2011 period and produced a similar result (R2 ¼ 0.66, Table 4) utilizing natural log transformed mean monthly chlorophyll-a

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H. Greening et al. / Estuarine, Coastal and Shelf Science xxx (2014) 1e16

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Fig. 5. a: Trends in mean annual TN concentrations (mg/L) in the 4 major bay segments of Tampa Bay. Horizontal lines represent target values established by the TBEP for the protection of seagrass resources in the bay. Data source: Environmental Protection Commission of Hillsborough County (EPCHC). b: Trends in mean annual TP concentrations (mg/L) in the 4 major bay segments of Tampa Bay. Horizontal lines represent target values established by the TBEP for the protection of seagrass resources in the bay. Data source: EPCHC.

values as the response variable and cumulative, 3-month TN loading as the predictor variable (Greening and Janicki, 2006). Interestingly for the 1985e2011 period, utilizing monthly mean TN concentrations as the predictor variable and inebay chlorophyll-a

concentrations as the response variable produced similar results (R2 ¼ 0.65, Table 4) as the relationship developed with TN loads. However, a poor relationship between inebay TN concentrations and antecedent TN loadings from the watershed still persists

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Fig. 6. Trends in mean annual chlorophyll-a concentrations (mg/L) in the 4 major bay segments of Tampa Bay (note different y-axis scales). Horizontal lines represent target values established by the TBEP for the protection of seagrass resources in the bay. Data source: EPCHC.

(R2 ¼ 0.29, Table 4). Based on the poor relationship of inebay TN concentrations to antecedent TN loads, Tampa Bay's management community has fully embraced TN loadings and delivery rates as the most appropriate unit for bay management as it relates more meaningfully to expected chlorophyll-a and water clarity conditions. The temporal variability in light attenuation (as measured by Secchi disk depth) in Tampa Bay is most significantly dependent

Table 4 Summary of ANOVA results relating (A) bay segment specific, monthly mean chlorophyll-a concentrations (mg/L) to cumulative, 3-month TN loads (kg), (B) bay segment specific, monthly mean chlorophyll-a concentrations (mg/L) to 3-month mean [TN] (mg/L), and (C) bay segment specific, monthly mean [TN] (mg/L) to cumulative, 3-month TN loads (kg) over the 1985e2011 period when data were available. Source

SS

df

MS

F

A) loge(Chlorophyll-a, mg/L) e TN Load Model (R2 ¼ 0.66, n ¼ 1277) Month 88.77 11 8.07 46.83 Bay Segment 50.45 3 16.82 97.58 Cumulative 3-month 16.46 4 4.11 23.87 TN Load (kg) (Bay Segment) Error 216.78 1276 0.17 B) loge(Chlorophyll-a, mg/L) e [TN] Model (R2 ¼ 0.65, n ¼ 1279) Month 167.61 11 15.24 87.38 Bay Segment 19.92 3 6.64 38.08 3-month Mean 13.63 4 3.41 19.53 ([TN], mg/L) (Bay Segment) Error 219.72 1260 0.17 C) loge ([TN], mg/L) e TN Load Model (R2 ¼ 0.29, n ¼ 1216) Month 4.73 11 0.43 3.56 Bay Segment 9.17 3 3.06 25.32 Cumulative 3-month TN Load 6.68 4 1.67 13.83 (kg) (Bay Segment) Error 144.52 1197 0.12

upon temporal variation in chlorophyll-a concentrations (Greening and Janicki, 2006). The observed relationship between chlorophylla concentration and Secchi disk depth in the four main bay segments is shown in Fig. 7. Decreases in light attenuation per unit change in chlorophyll-a concentrations are reduced when concentrations are greater than 10 mg/L. Given this relationship, it is not surprising that there have been significant increasing trends in Secchi disk depth in all four bay segments (Fig. 8). As found for chlorophyll-a and nutrient concentrations, the increasing trends in monthly mean Secchi disk depths for each of the bay segments are all highly significant (P < 0.001).

p <0.0001 <0.0001 <0.0001

<0.0001 <0.0001 <0.0001

<0.0001 <0.0001 <0.0001 Fig. 7. Relationship between mean monthly Secchi disk depth (m) and chlorophyll-a concentration (mg/L) in Tampa Bay. Data source: EPCHC.

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While the Secchi disk depth continued to increase in a relatively monotonic fashion, the chlorophyll-a concentration varied from year to year. Previous analyses have demonstrated that, while both turbidity and color contributed to the overall absolute light attenuation, neither explained the temporal variation in Secchi disk depth. There is no apparent temporal pattern to that observed for Secchi disk depth in either the turbidity or the color data. However, the observed enhanced growth patterns in seagrass extent and water clarity appear to be consistent with a positive feedback response as described by Kemp et al. (2005), Bos et al. (2007), van Katwijk et al. (2010), and van der Heide et al. (2011). The positive feedback response posits that seagrasses are able to trap and stabilize suspended sediments, which in turn improves water clarity and seagrass growth conditions. Kemp et al. (2005), evaluating eutrophic conditions and trends in Chesapeake Bay, found that ecosystem responses to changes in nutrient loading are complicated by non-linear feedback mechanisms including particle trapping and binding by benthic plants that increase water clarity. Dissolved oxygen (DO) concentrations have also exhibited a response to management since the 1980s. Santos and Simon (1980) reported that in the nearshore waters along the western shore of Hillsborough Bay anoxia could be found in a very predictable manner and with a resulting defaunation of the benthic community. Examination of bottom DO data from the period preceding more intense bay nutrient management (ca. 1970s) shows more than 30% of the samples collected exhibit anoxic conditions (DO < 0.5 mg/L). In a similar fashion to the observed changes in water quality conditions described above following the implementation of advanced wastewater treatment, the frequency of these low DO conditions declined to ca. 10% in the 1980s. Since the mid-1990s, the relatively few, low DO observations in the bay (i.e. concentrations <4 mg/L) appear to be more influenced by physical factors (e.g. shallow, high temperature flats or deep, dredged

11

shipping channels) rather than as a result of nutrient eutrophication processes (Janicki Environmental, Inc. 2011). 5.3. Primary and secondary production Tampa Bay has an extensive four-decade long monthly record of phytoplankton biomass and primary production. The biomass record is baywide, but the production record is limited to the upper half of the bay (Johansson, 2005). Phytoplankton production measurements in the 1980-1989 period were conducted using the classic in situ 14C method developed by Steemann-Nielsen (1952) and modified by Strickland and Parsons (1968). Primary production estimates for 1953 and 2010-2013 time periods were estimated from production/biomass ratios. Chlorophyll-a concentration measurements from Marshall (1956) were used to develop the 1953 carbon production estimate. Consistent and baywide estimates of seagrass area coverage are available through mapping of aerial photographs with on-the-ground confirmation on a near two-year interval starting in 1988. Records of Tampa Bay phytoplankton and seagrass communities prior to and during the period of distinct increased eutrophication are less consistent, but sufficient to develop a general understanding of conditions present in the 1950s and the subsequent phase leading to peak eutrophication in the estuary. Temporal and spatial trends of the primary production rates and biomass for the phytoplankton and seagrass communities were compiled and examined for the seven decades from the 1950se2010s. Baywide phytoplankton production per m2 (Fig. 9) increased by 55% between 1950 and 1980. Productivity in the most impacted bay segment, Hillsborough Bay, showed a similar pattern. Conversely, baywide seagrass production during this phase was reduced by nearly 50%, and in Hillsborough Bay seagrasses were completely eliminated. The seagrass decline has been attributed to

Fig. 8. Trends in mean annual Secchi disk depth (m) for the 4 major bay segments of Tampa Bay. Horizontal lines represent target values established by the TBEP for the protection of seagrass resources in the bay. Data source: EPCHC.

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several factors including a degraded light environment due to the increase in phytoplankton production and biomass. During the recovery phase, from 1980 to 2010, trends of the two communities were reversed; baywide phytoplankton production declined by more than 30% and seagrass production increased by about 50%. In Hillsborough Bay, seagrass is once again present. Thus, the trend of these two carbon-producing communities during the recovery phase follows a trend in an opposite direction but in a fairly parallel path as seen during the eutrophication phase. Fisheries-independent monitoring of juvenile and small-adult fishes has been conducted by the Florida Fish and Wildlife Conservation Commission's Fish and Wildlife Research Institute since 1988. Indices of relative abundance show significant interannual differences, responses to annual levels of freshwater inflow, and changes after a legislatively-mandated commercial net ban was enacted in 1995 (Matheson et al., 2005). Although fisheries data are not available prior to the initiation of water quality and seagrass improvements in the 1980s, observations from recreational anglers confirm their belief that seagrass recovery has fostered improved fishing in Tampa Bay (Brown, 2014). 5.4. Seagrass Seagrasses have been identified as a key environmental resource in Tampa Bay because of their critical importance in providing habitat for large numbers of fish and shellfish species, their sensitivity to water quality degradation, their roles in nutrient cycling and as detrital matter sources, improving the stability of bottom sediments, and the fact that they serve as food sources for manatees, sea turtles and other wildlife. Consistent methods to estimate seagrass areal extent were first initiated in 1982 in Tampa Bay, and have been conducted on a regular basis since approximately 1988. Therefore, there are no estimates of seagrass coverage immediately prior to the large point source nutrient loading reductions other than a single estimate from ca. 1954 (Fig. 10). Methods rely on photo-interpretation of aerial photography acquired and analyzed in a similar manner since the inception of the mapping program by the Southwest Florida Water Management District. In the contemporary period, estimates occur on a near, 2-yr basis but have been contingent on budget availability (e.g. 1998 gap in Fig. 10). On a long-term basis, changes in seagrass cover in the bay have reflected changes in water quality. Analysis of aerial photographs,

Fig. 9. Estimated Tampa Bay carbon production by phytoplankton and seagrass communities over historical and contemporary time periods when data were available, baywide and for the Hillsborough Bay segment.

habitat maps, and the extent of urbanization show that seagrass cover in Tampa Bay has fluctuated markedly during the roughly sixdecade period (1950e2012) for which baywide photography is available (Fig. 10). Cover declined by an estimated 8900 ha (or about 50%; Haddad, 1989) between the early 1950s and early 1980s, during a period characterized by widespread physical impacts (e.g., dredging and filling) and increasingly poor water quality (Johansson and Greening, 2000). Cover then increased by about 5258 ha (or about 38%) from the early 1980s through 2012, as the magnitude and frequency of physical impacts were reduced and water quality improved. An inverse relationship between the extent of urbanization and seagrass cover persisted from 1940 through 1985, after which both increased urbanization levels and seagrass expansion have been observed (Crane and Xian, 2006). The increase in seagrass coverage observed since 1982 was interrupted in the late 1990s, when a loss of more than 800 ha between 1996 and 1998 was recorded. This loss is coincident with ~ o year in 1997e1998, increased heavy winter rains of an El Nin chlorophyll-a concentrations (Fig. 6) and decreased clarity (as indicated by Secchi disk depth; Fig. 8). However, seagrass areal extent estimates returned to pre-1998 levels within four years, and estimates have been increasing with every subsequent measurement (Fig. 10). The baywide seagrass recovery trajectory appears to have ~ o setback. Prior to 1998, seagrass changed after the 1998 El Nin recovery was occurring at a rate of ~163 ha per year, while after this event seagrass recovery is now observed to be at a rate of ~300 ha per year (Fig. 10). An ANCOVA indicated that these rates were significantly different (P ¼ 0.008). This enhanced recovery trajectory during the more recent period may be related to positive feedbacks (e.g., Kemp et al., 2005) from a combination of improved water clarity, reduced sediment resuspension, and bay management activities observed during this period. Seagrass coverage gains were further investigated in response to meeting the established, bay segment specific chlorophyll-a concentration and light attenuation targets for Tampa Bay. A simple logistic regression was performed to determine whether seagrass coverage increases during the available period of record are likely

Fig. 10. Total seagrass coverage (ha) in Tampa Bay circa 1950 through 2012. Separate regression fits of seagrass coverage over time and among the pre-1998 and post~ o periods. Seagrass coverage estimates were derived from photo1998 El Nin interpretation of aerial photographs consistently acquired and analyzed by the SWFWMD. An ANCOVA found a significant difference between the regression slopes of the two time periods (n ¼ 13, P ¼ 0.008). Data sources: SWFWMD Haddad 1989.

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when one or both of the targets were met. For the 1988e2012 period, the overall probability of observing seagrass coverage increases in the bay was 43% (20.7e68.4%, 95% C.I.). However, when one or both targets were met in the preceding year, then the resulting probability of observing gains in seagrass coverage increased significantly to 81% (58.8e92.7%, 95% C.I.) and 85%, (54.9e96.1%, 95% C.I.), respectively. These results suggest that continually and consistently meeting bay segment-specific water clarity targets for chlorophyll-a concentration and light attenuation in a given year will likely foster continued increases in seagrass coverage in Tampa Bay. The established water clarity management targets have garnered considerable buy-in from TBEP partners as attainable goals, and thus reflect both desired ecological endpoints and achievable societal actions necessary to meet long-term seagrass recovery goals. Because of positive increases in seagrass coverage, regulators have ruled that attaining these targets provides reasonable assurance for meeting future recovery goals. 6. Discussion The observed relationship between increased urbanization in coastal areas and decreased estuarine condition has been well documented (NRC, 2000; Valiela et al., 2000; Cloern, 2001; Garnier et al., 2002; Bricker et al., 2007; Duarte et al., 2013; Valiela and Bartholomew, 2014). In contrast to many coastal systems throughout the world, the water quality and seagrass improvements observed starting in 1985 in Tampa Bay have occurred simultaneously with an increase in the extent of urbanized land and an additional 1.1 M people (a population increase of 40%) living in the watershed during this same time period. The many projects and actions completed by public and private sectors appear to have offset nutrient loading contributions (both wastewater and nonpoint sources) typically contributed by increased population and urbanization. Restoration and recovery trajectories following nutrient loading reduction are often convoluted. Duarte et al. (2009) evaluated the response to nutrient reduction in four European coastal ecosystems (the Netherlands, Germany, Denmark and Latvia/Estonia), all of which showed both statistically significant eutrophication in the 1970s-1980s and recovery phases starting in the 1990s. Each ecosystem displayed a different recovery trajectory, and all four have, to date, failed to return to the reference condition after nutrient reduction to pre-eutrophication levels. Based on the results of their evaluation, Duarte et al. (2009) developed four idealized trajectories of chlorophyll-a concentration, as an indicator of ecosystem status, and nutrient inputs to coastal ecosystems under increasing and decreasing nutrient inputs. They submit that the expectation that ecosystems will return to the original conditions tracking reversed trajectories following reduced nutrient inputs projections may be fundamentally flawed, due to the consequences of shifting baselines which are occurring at the same time (i.e., overfishing, climate change). These baseline shifts cause the coastal ecosystem to drift away from their ‘reference’ condition. Our results indicate that recovery of Tampa Bay appears to be closely following the ‘regime shift’ trajectory proposed by Duarte et al. (2009). The ecosystem improvements observed in Tampa Bay in the mid-1980s appear to be returning Tampa Bay back to a 1950s reference state. Water quality parameters (chlorophyll-a concentration, water clarity as indicated by Secchi disk depth, nutrient concentrations, and dissolved oxygen) and seagrass coverage exhibited significant improvements within several years of wastewater nutrient load abatement and are approaching baseline, relatively pre-disturbance, conditions observed in the 1950s.

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Although Tampa Bay's recovery to date is on a positivedand possibly enhanceddtrajectory, maintaining that trajectory will require continued action, assessment and adjustment. Groffman et al. (2006) found that local, short-term thresholds, which are what are most commonly managed, are constantly shifting due to changes in external factors such as climate or land use changes. Similarly, following evaluation of 28 long-term datasets, Carstensen et al. (2011) found that individual ecosystems exhibit unique chlorophyll-a concentration to TN relationships, such as what is exhibited in Tampa Bay's different major bay segments. Carstensen et al. (2011) further state that changes are likely derived from largescale forcing associated with global change, and they imply that current chlorophyll-a and nutrient relationships cannot be used to predict future relationships. Sea level rise scenarios developed for Tampa Bay show the potential for the need to revise habitat restoration strategies over time, as well as nutrient management plans (Sherwood and Greening, 2014). In Tampa Bay, the shift from a turbid phytoplankton-based system to a clear water seagrass-based system in the 1980s has not only resulted in improved ecological conditions in Tampa Bay, but is also contributing to increased economic value of the region through enhanced ecosystem services. Annual nitrogen removal from increased seagrass extent is conservatively estimated to have increased by US $7.4 M between 1982 and 2010 (Russell and Greening, 2013). A recently-completed economic evaluation of Tampa Bay (Tampa Bay Regional Planning Council Economic Analysis Program, 2014) found that almost half of the jobs in the Tampa Bay watershed are influenced by the presence of the Bay, and one out of every five jobs within the watershed is dependent on a clean, healthy bay. A healthy Tampa Bay accounts for 13% (US $22B) of the local economy. 7. Conclusions Two broad conclusions can be drawn from the Tampa Bay example. First, under certain conditions some of the major impacts of estuarine eutrophication and watershed development can be reversed. The second conclusion is that continued watershed-based nutrient management is critical for addressing the impacts brought about by an increasing human population. Key management elements that have contributed to the observed improvements in Tampa Bay during the past several decades include:  Development of numeric water quality targets. The water quality targets were developed to meet a quantitative long-term goal of restoring seagrass coverage to baseline 1950s levels. Too often ecosystem management plans are built on imprecise or non-quantitative goals resulting in a lack of focus that is difficult to overcome. Rather, we found that establishing quantitative goals early in the process resulted in meaningful participation by the stakeholders as evidenced by their voluntary participation in the comprehensive nutrient management strategy for Tampa Bay. The availability of long-term monitoring data, and a systematic process for using the data to evaluate the effectiveness of management actions, has allowed managers to track progress and make adaptive changes when needed. Annual reporting to the community and regulatory agencies on the attainment of water quality targets (Table 5) has been an essential part in continuing public and private entity engagement in the Tampa Bay nutrient management strategy.  Citizen involvement. The initial reductions in TN loads, which occurred in the late 1970s and early 1980s, were a result of state regulations that were developed in response to citizens' call for action. Improved water clarity and better fishing and swimming

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conditions were identified as primary goals by citizens again in the early 1990s, and led to development of numeric water quality targets and seagrass restoration goals. More recent citizen actions, from pet waste campaigns to support for reductions in residential fertilizer use, are important elements of the nitrogen management strategy.  Collaborative actions. In addition to numerous other collaborative ventures that have benefitted Tampa Bay, the public/private, stakeholder-driven TBNMC, which includes more than 45 participating organizations, has implemented 300 þ nutrient reduction projects. These projects have addressed stormwater treatment, fertilizer manufacturing and shipping, agricultural practices, reclaimed water use, and atmospheric emissions from local power stations, providing more than 450,000 kg of TN load reductions since 1995.  State and federal regulatory programs. Regulatory requirements, such as state statutes and rules requiring compliance with advanced wastewater treatment (AWT) standards by municipal sewerage works, have played a key role in Tampa Bay management efforts. The technical basis and implementation plan of the Tampa Bay nitrogen management strategy have been

developed in cooperation with state and federal regulatory agencies, and the strategy has been recognized by them as an appropriate tool for meeting water quality standards, including federally-mandated total maximum daily loads (TMDLs) and numeric nutrient criteria. Local governments, municipalities and private businesses around the country realize the importance of a healthy watershed and bay environment to the economy of their regions. Many are also facing requirements to meet federal, state and local water quality regulations. In Tampa Bay, local communities and industries developed voluntary water quality goals and nutrient loading targets to support recovery of clear water and underwater seagrasses in the mid-1990s, and have implemented more than 300 projects since 1996 to help meet the nutrient loading targets developed for Tampa Bay. Their collective efforts, starting with significant wastewater point source reductions and continuing with nutrient loading reductions from atmospheric, industrial and community sources, have resulted in a present-day Tampa Bay which looks and functions much like it did in the relatively pre-disturbance 1950s period.

Table 5 Average annual chlorophyll-a concentration threshold attainment for the four major bay segments relative to major nutrient management actions that occurred throughout the watershed from 1974 to 2013. White (no) indicates years when a bay segment-specific threshold was not attained, while green (yes) indicates years when a threshold was attained. Data source: EPCHC.

Please cite this article in press as: Greening, H., et al., Ecosystem responses to long-term nutrient management in an urban estuary: Tampa Bay, Florida, USA, Estuarine, Coastal and Shelf Science (2014), http://dx.doi.org/10.1016/j.ecss.2014.10.003

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Editors' Note The widespread eutrophication of coastal waters has been the subject to much scientific and management effort, yet we have too few examples where there is a substantive scientific record, and sustained tracking of management actions. In this issue Greening and colleagues review the time courses of ambient conditions, describe what was done to remediate severely eutrophic water quality, and demonstrate the recovery trajectory of a number of variables useful to track ecosystem responses. In addition, a compelling aspect of the paper is that it also describes the social side of the recovery, i.e., what was needed to bring the community and political action to perceive and act upon the issues, and develop a plan to address the problems. The improvement in water quality and environmental conditions currently taking place in Tampa Bay is an excellent example of what can be achieved with the combination of basic understanding of the scientific issues, application of reasonable technological advances, and the marshaling of popular support for action. Acknowledgments The Tampa Bay Nitrogen Management Strategy is the product of many years and multiple participants, primary among them the public and private partners of the Tampa Bay Nitrogen Management Consortium. Development of this Strategy would not have been possible without the long-term water quality and seagrass monitoring programs conducted by the Environmental Protection Commission of Hillsborough County and the Southwest Florida Water Management District. Comments and recommendations from two anonymous reviewers and I. Valiela, ECSS Editor, have greatly improved the manuscript. Funding for this work is provided by the Tampa Bay Estuary Program partners, including the US Environmental Protection Agency, Southwest Florida Water Management District, the counties of Hillsborough, Manatee and Pinellas, the cities of Clearwater, St. Petersburg, and Tampa, and Tampa Bay Water. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.ecss.2014.10.003. References Anderson, D.M., Glibert, P.M., Burkeholder, J.M., 2002. Harmful algal blooms and eutrophicationdnutrient sources, composition, and consequences. Estuaries 25, 704e726. Boesch, D., Brinsfield, R.B., Magnien, R.E., 2001. Chesapeake Bay eutrophication: scientific understanding, ecosystem restoration, and challenges for agriculture. J. Environ. Qual. 30, 303e320. Bos, A.R., Bouma, T.J., de Kort, G.L.J., van Katwijk, M.M., 2007. Ecosystem engineering by annual intertidal seagrass beds: sediment accretion and modification. Estuar. Coast. Shelf Sci. 74, 344e348. Boynton, W.R., Hodgkins, C.L.S., O'Leary, C.A., Bailey, E.M., Bayard, A.R., Wainger, L.A., 2014. Multi-decade responses of a tidal creek system to nutrient load reductions: Mattawoman Creek, Maryland USA. Estuaries Coasts 37 (Suppl. 1), S111eS127. http://dx.doi.org/10.1007/s12237-013-9690-4. Bricker, S.B., Clement, C.G., Pirhalla, D.E., Orlando, S.P., Farrow, D.G.G., 1999. National Estuarine Eutrophication Assessment: Effects of Nutrient Enrichment in the Nation's Estuaries. Special Projects Office and the National Centers for Coastal Ocean Science, National Ocean Service, National Oceanic and Atmospheric Administration, Silver Spring, MD. Bricker, S., Longstaff, B., Dennison, W., Jones, A., Boicourt, K., Wicks, C., Woerner, J., 2007. Effects of Nutrient Enrichment in the Nation's Estuaries: a Decade of Change. NOAA Coastal Ocean Program Decision Analysis Series No. 26. National Centers for Coastal Ocean Science, Silver Spring, Maryland, p. 328. Brown, D.A., May 2014. Tampa Bay seagrass resurgence. Fla. Sportsman 70e76. Burns, J., 2008. Toxic cyanobacteria in Florida waters. In: Hudnell, H.K. (Ed.), Proceedings of the International Symposium on Cyanobacterial Harmful Algal Blooms: Advances in Experimental Medicine and Biology, pp. 117e126.

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