Ecosystem responses to long-term nutrient management in an urban
estuary: Tampa Bay, Florida, USA
, A. Janicki
, E.T. Sherwood
, R. Pribble
, J.O.R. Johansson
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
Accepted 7 October 2014
Available online 22 October 2014
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 in-
crease of more than 1 M people living within the Tampa Bay metropolitan area. Water quality (chlo-
rophyll-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, phytoplankton-
based system to a clear water, seagrass-based system that began in the 1980s following comprehen-
sive 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.
A primary water quality challenge facing estuaries throughout
the world is cultural eutrophication ea 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 macro-
algae (Nixon, 1995; Bricker et al., 1999, 2007; NRC, 2000; Cloern,
2001; Duarte et al., 2013). Such blooms affect estuarine ecosys-
tems 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
habitats. Several bloom-forming phytoplankton species also pro-
duce 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,
E-mail address: firstname.lastname@example.org (H. Greening).
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Estuarine, Coastal and Shelf Science 151 (2014) A1eA16
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 ‘super-
bloom’of microalgae. This severe freeze resulted in a signiﬁcant
die-back of macroalgae that in turn increased nutrient concentra-
tions 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 Mary-
land/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 deﬁni-
tions 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, Massa-
chusetts, 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 Mat-
tawoman 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 man-
agement 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 tra-
jectories, and identify key science, management, and policy ele-
ments 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 develop-
ment of the scientiﬁc basis for quantifying restoration and protec-
tion 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
2. Tampa Bay characteristics
Tampa Bay is a large (water surface area of 1036 km
(mean depth 4 m), Y-shaped embayment located on the west-
central 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 km
bathymetry has been modiﬁed by the construction and mainte-
nance of an extensive network of shipping channels, dredged to
depths of about 13 m. Model-based estimates of bay-wide resi-
dence times range from weeks to months and are primarily inﬂu-
enced 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 environ-
mental 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 fresh-
water 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 waste-
water treatment plant. As a result, nutrient loading to Hillsborough
Bay is larger than any other bay segment. Circulation in Hills-
borough Bay is largely inﬂuenced by these inputs as well as a sig-
niﬁcant 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 charac-
terized 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 Bayas 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. Signiﬁ-
cant 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
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16A2
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 popu-
lation 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 fa-
cilities with bulk commercial shipping interests occur in the upper
and lower bay and are an important component of the local
The Tampa Bay drainage basin differs from many other estuaries
because extensive phosphate deposits are actively mined for fer-
tilizer 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
Fig. 1. Tampa Bay location and 2010 land use map of the watershed. Source: Southwest Florida Water Management District (SWFWMD).
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16 A3
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 phos-
phorus 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 sug-
gesting 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 refer-
enced 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
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 ehistorical 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
Characteristics of the four major bay segments in Tampa Bay.
Bay segment Surface
Lower Tampa Bay 247 1200 4 298
Middle Tampa Bay 310 1166 4 952
Old Tampa Bay 200 548 3 774
Hillsborough Bay 105 306 3 2797
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.
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).
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16A4
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 macro-
fauna 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 phyto-
plankton 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. Eutro-
phication 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 eA 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 imple-
mentation of state legislation known as the Grizzle-Figg Act (Flor-
ida 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. Peters-
burg 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 re-
quirements for non-agricultural stormwater systems, reducing
nutrient and sediment loading from urban and residential
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
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
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 re-
covery. 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/pri-
vate 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 Part-
nership for Progress, consisted of more than 100 projects that
collectively reduced or precluded nitrogen discharges to the bay by
more than 224,00 0 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 par-
ticipants 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. Envi-
ronmental Protection Agency (EPA) and the Florida Department of
Environmental Protection (FDEP) to dramatically reduce overall
emissions from Tampa Electric Company's power plants. Its Selec-
tive 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 NO
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 Agricul-
ture and Community Services has been working with stakeholders
to develop Best Management Practices (BMPs) speciﬁc to their
agricultural practices (http://www.freshfromﬂorida.com/Divisions-
Ofﬁces/Agricultural-Water-Policy/). The inﬂuence of phosphate
mining on Tampa Bay nutrient loadings are regulated by the
Timeline of management events that have coincided with Tampa Bay's recovery.
1980 Grizzle-Figg Act requiring TN reductions from wastewater
treatment plants implemented
1985 Stormwater permitting implemented
1991 Tampa Bay Estuary Program established
1996 Tampa Bay Nitrogen Management Consortium (TBNMC) formed
2002 FDEP accepts TBNMC Action Plan as meeting regulatory requirements
2004 Power plant repowerings begin
2010 FDEP accepts TBNMC recommendations of TN loading allocations
to individual sources
2012 Tampa Bay Estuary Numeric Nutrient Criteria recommendations
enacted by the State
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16 A5
National Pollutant Discharge Elimination System (NPDES). The
NPDES permitting process in combination with signiﬁcant re-
ductions 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 Man-
agement 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 rec-
ommended 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 an-
alyses peer-reviewed by the TBEP, its partners, and state and federal
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 res-
idential 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 collabora-
tion 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 I
(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 I
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 measure-
ments), 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 vari-
ations in response to these factors in the four largest bay segments.
The model that provided the best ﬁt (highest R
) to the observed
water clarity data took the form:
is the depth to which 20.5% of surface irradiance pene-
trates in month tand bay segment s;C
is the average chlorophyll-
a concentration in month tand bay segment s; and
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 (R
¼0.67). 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 concentra-
tion targets developed using this process, which range from 4.6
L to 13.2
g/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
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16A6
average of more than 20.5% of subsurface irradiance (I
) to reach
target depths (the estimated depths to which seagrasses grew in
the early 1950s) in three of the four largest bay segments. A ni-
trogen 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 eval-
uating 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 sour-
ces, 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 at-
mospheric 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 dis-
charges 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.
Many of these facilities are associated with phosphate mining ac-
tivities 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 fertil-
Groundwater inputs along the shoreline also contribute nitro-
gen 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 water-
shed. 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 TampaBay 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 same-
month 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 use-
speciﬁc 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 cit-
rus 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).
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16 A7
On a baywide basis, there were marked responses in the envi-
ronment 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 un-
derstand 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) depo-
sition 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
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 capitaTN loadwas approximately 6.6 kg/person/yr. From1985 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 TNloads 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
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 re-
ductions (Fig. 5a, b). These reductions have resulted in TN and TP
concentrations that have been consistently lower by at least 50%
since a 1998 El Ni~
no heavy rainfall period. The observed trends
were examined using the Seasonal Kendall Tau method on mean
monthly data during the 1974e2013 period. Both TN and TP con-
centrations 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 con-
centrations 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 accu-
mulated 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 regenera-
tion processes strongly impacted water column nitrogen concen-
trations. 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 sur-
mised that longer-term sustained reductions would lead toreduced
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
no years), and to occasional summer nuisance algae blooms
(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-aconcentrations
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 concen-
tration have been suggested as the time needed for internal pro-
cesses 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
Relationships in chlorophyll-a concentrations, nutrient load-
ings, 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 rela-
tionship between monthly mean chlorophyll-a concentrations and
cumulative, 3-month TN loading to each of the 4 major bay seg-
¼0.69) was the most robust predictor for bay manage-
ment purposes. The empirical model was updated for the
1985e2011 period and produced a similar result (R
¼0.66, Table 4)
utilizing natural log transformed mean monthly chlorophyll-a
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
Point sources 60.3 19.5
Nonpoint sources 23.9 57.4
Atmospheric deposition 10.8 20.4
Fertilizer handling losses 4.9 0.5
Groundwater &Springs 0.1 2.1
Total 100 (8,984,760 kg) 100 (3,410,582 kg)
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16A8
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
¼0.65, 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
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.
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16 A9
¼0.29, 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
The temporal variability in light attenuation (as measured by
Secchi disk depth) in Tampa Bay is most signiﬁcantly dependent
upon temporal variation in chlorophyll-a concentrations (Greening
and Janicki, 2006). The observed relationship between chlorophyll-
a concentration and Secchi disk depth in the four main bay seg-
ments is shown in Fig. 7. Decreases in light attenuation per unit
change in chlorophyll-a concentrations are reduced when con-
centrations are greater than 10
g/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).
Fig. 6. Trends in mean annual chlorophyll-a concentrations (
g/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.
Summary of ANOVA results relating (A) bay segment speciﬁc, monthly mean
chlorophyll-a concentrations (
g/L) to cumulative, 3-month TN loads (kg), (B) bay
segment speciﬁc, monthly mean chlorophyll-a concentrations (
g/L) to 3-month
mean [TN] (mg/L), and (C) bay segment speciﬁc, monthly mean [TN] (mg/L) to cu-
mulative, 3-month TN loads (kg) over the 1985e2011 period when data were
Source SS df MS F p
g/L) eTN Load Model (R
Month 88.77 11 8.07 46.83 <0.0001
Bay Segment 50.45 3 16.82 97.58 <0.0001
TN Load (kg)
16.46 4 4.11 23.87 <0.0001
Error 216.78 1276 0.17
g/L) e[TN] Model (R
Month 167.61 11 15.24 87.38 <0.0001
Bay Segment 19.92 3 6.64 38.08 <0.0001
13.63 4 3.41 19.53 <0.0001
Error 219.72 1260 0.17
([TN], mg/L) eTN Load Model (R
Month 4.73 11 0.43 3.56 <0.0001
Bay Segment 9.17 3 3.06 25.32 <0.0001
Cumulative 3-month TN Load
6.68 4 1.67 13.83 <0.0001
Error 144.52 1197 0.12
Fig. 7. Relationship between mean monthly Secchi disk depth (m) and chlorophyll-a
g/L) in Tampa Bay. Data source: EPCHC.
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16A10
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 atten-
uation, 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 sta-
bilize 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 compli-
cated by non-linear feedback mechanisms including particle trap-
ping 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 commu-
nity. 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 imple-
mentation 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
shipping channels) rather than as a result of nutrient eutrophica-
tion 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 re-
cord is baywide, but the production record is limited to the upper
half of the bay (Johansson, 2005). Phytoplankton production mea-
surements in the 1980-1989 period were conducted using the
classic in situ
C method developed by Steemann-Nielsen (1952)
and modiﬁed by Strickland and Parsons (1968). Primary produc-
tion 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 esti-
mates 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 phyto-
plankton and seagrass communities prior to and during the period
of distinct increased eutrophication are less consistent, but sufﬁ-
cient 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 m
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.
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16 A11
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 Con-
servation 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).
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 sensi-
tivity 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 mana-
tees, 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,
habitat maps, and the extent of urbanization show that seagrass
cover in Tampa Bay has ﬂuctuated markedly during the roughly six-
decade 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
heavy winter rains of an El Ni~
no year in 1997e1998, increased
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 measure-
ment (Fig. 10).
The baywide seagrass recovery trajectory appears to have
changed after the 1998 El Ni~
no setback. Prior to 1998, seagrass
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 (P¼0.008). This enhanced recovery trajec-
tory 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 manage-
ment activities observed during this period.
Seagrass coverage gains were further investigated in response to
meeting the established, bay segment speciﬁc chlorophyll-a con-
centration 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. 9. Estimated Tampa Bay carbon production by phytoplankton and seagrass com-
munities over historical and contemporary time periods when data were available,
baywide and for the Hillsborough Bay segment.
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-
1998 El Ni~
no periods. Seagrass coverage estimates were derived from photo-
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 (n¼13 , P¼0.008). Data sources: SWFWMD Haddad 1989.
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16A12
when one or both of the targets were met. For the 1988e2012
period, the overall probability of observing seagrass coverage in-
creases 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.
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 improve-
ments 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
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 concentra-
tion, as an indicator of ecosystem status, and nutrient inputs to
coastal ecosystems under increasing and decreasing nutrient in-
puts. 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 ‘refer-
ence’condition. Our results indicate that recovery of Tampa Bay
appears to be closely following the ‘regime shift’trajectory pro-
posed 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 param-
eters (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.
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 large-
scale 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.
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 de-
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 participa-
tion 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 effective-
ness 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 engage-
ment 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
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16 A13
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 citi-
zen actions, from pet waste campaigns to support for reductions
in residential fertilizer use, are important elements of the ni-
trogen management strategy.
Collaborative actions. In addition to numerous other collabo-
rative ventures that have beneﬁtted Tampa Bay, the public/pri-
vate, stakeholder-driven TBNMC, which includes more than 45
participating organizations, has implemented 300 þnutrient
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 re-
quirements, such as state statutes and rules requiring compli-
ance 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 tar-
gets 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
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.
H. Greening et al. / Estuarine, Coastal and Shelf Science 151 (2014) A1eA16A14
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 combi-
nation of basic understanding of the scientiﬁc issues, application of
reasonable technological advances, and the marshaling of popular
support for action.
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 Manage-
ment 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://
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