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Impacts of Urbanization and Development on Estuarine Ecosystems
and Water Quality
Lauren A. Freeman
1
&D. Reide Corbett
2
&Allison M. Fitzgerald
3
&Daniel A. Lemley
4
&Antonietta Quigg
5
&
Cecily N. Steppe
6
Received: 11 June 2018 /Revised: 24 April 2019 /A ccepted: 11 June 2019
#This is a U.S. government work and its text is not subject to copyright protection in the UnitedStates; however, its text may be subject to foreign copyright
2019
Abstract
Urbanization and human-led development have increased more rapidly along shorelines and in coastal watersheds than inland
regions overthe past century. The result of major land use changes for bothurban tracts and agriculture to serve the urban areas, as
well as infrastructure development is increased runoff carrying sediments, nutrients, pollutants, pharmaceuticals, and toxins
downstream to estuarine systems. The increased runoff levels are only the tip of the iceberg, with human development resulting
in increased fecal bacteria from urbanization and excess nutrients from agriculture leading to harmful algal blooms. Estuaries act
as a natural filter between land and sea, but have been overloaded by the influx of sediments and pollutants in recentdecades. As a
result, there have been a variety of impacts to estuarine ecosystems and water quality including increased sediment load,
eutrophication, harmful algal blooms, fecal bacteria, as well as shellfish and fisheries declines. In some estuarine systems, the
reduction in light penetration to the benthos has led to the loss of seagrasses. In others, seasonal hypoxia is a visible symptom of
prolonged eutrophication. There is a need to augment long-term monitoring techniques with new technologies and data process-
ing methods to better understand the current state of estuaries and work towards mitigating human impacts on estuarine
ecosystems and water quality.
Keywords Estuarine ecosystems .Wa ter quali ty .Urbanization .Human i mpacts .Oysters .Suspended sediments .Harmful algal
blooms
Introduction
Urbanization is transforming the world’s coastlines on timescales
of years to decades. Human population centers tend to be near
rivers and coastlines. In 2010, 123.3 million people, or 39% of
the US population, lived in counties directly on the shoreline
(Fig. 1). This population is expected to increase by about 10
million people, or 8%, from 2010 to 2020 (https://oceanservice.
noaa.gov/facts/population.html). While less than 20% of land in
the USA is in a coastal watershed county, these counties are
home to more than half of the population (53%). From 1970 to
2010, coastal shoreline counties added 125 people per square
mile, over three times the national average of 39 people per
square mile (http://stateofthecoast.noaa.gov). As human
populations continue to grow and urbanization escalates in
coastal and watershed counties, waterways and aquatic
ecosystems are often adversely affected. Estuaries, the natural
buffer zone between rivers and the ocean, are among the most
Communicated by Kenneth L. Heck
*Lauren A. Freeman
lauren.a.freeman@navy.mil
1
Naval Undersea Warfare Center Division Newport Code 8511,
Newport, RI, USA
2
Coastal Studies Institute, East Carolina University, Wanchese, NC,
USA
3
Biology Department|, New Jersey City University, Jersey City, NJ,
USA
4
Botany Department and the Institute for Coastal and Marine
Research, Nelson Mandela University, Port Elizabeth 6031, South
Africa
5
Marine Biology Department, Texas A&M University at Galveston,
Galveston, TX, USA
6
Department of Oceanography, US Naval Academy, Annapolis, MD,
USA
Estuaries and Coasts
https://doi.org/10.1007/s12237-019-00597-z
impacted waterways and aquatic ecosystems. Estuaries are
particularly vulnerable because they often have a large
watershed, much greater than their own area. Impacts of
urbanization on estuaries include increases in sediment, nutrient,
and fecal microbial loading and subsequent shifts in water quality,
potentially leading to harmful algal blooms; changes in streamflow
and salinity; and the subsequent effects of these environmental
shifts on plankton, marshes, seagrasses,shellfish,andfishwithin
the estuary (Dauer et al. 2000; Mallin et al. 2000;Alberti2005;
Carle et al. 2005; Campos and Cachola 2007; Paerl et al. 2014;
Lemley et al. 2018a).
Water quality further impacts quality of life for humans living
near estuaries as events like harmful algal blooms and high
turbidity may limit recreational use of the waters, and could incur
an economic cost as well. Despite the value of the ecosystem
services provided by estuaries, most urban design planning takes
little account for neighboring estuarine waterways. Rapid urbani-
zation in the past century has put immense stress on these systems
that has resulted in sometimes dramatic shifts in water quality and
fish/shellfish stocks, with some oyster grounds completely extir-
pated due to microbial pathogens and historical levels a distant
memory (Figs. 2and 3). Those shellfish beds that are still surviving
are often closed to fishery collections due to microbial pathogens. It
is thus critical to understand the specific effects of urbanization on
estuarine waterways and ecosystems to mitigate the potential harm
caused by this process. This is more imperative now than ever
Fig. 1 US population density by county in 2010 (a) and population change by county from 1990 to 2000 (b), courtesy US Census Bureau. Note higher
population densities in coastal counties as well as more rapid population growth along coasts and in watersheds in the twenty-first century
Estuaries and Coasts
given many estuaries are now beyond their capacity to assimilate
or process these inputs, although that the same pollutants, excess
nutrient loads, and toxic materials make their way downstream to
the oceans.
Many estuaries have monitoring systems in place in response
to the stress of human impacts and the intrinsic value of these
systems. In 1987, the Environmental Protection Agency (EPA)
National Estuary Program recognized 28 estuaries of national
significance along the US Atlantic, Gulf, and Pacific coasts and
in Puerto Rico (https://www.epa.gov/nep). Several years later, the
National Oceanographic and Atmospheric Administration
(NOAA) National Estuarine Research Reserve System, a net-
work of 29 coastal sites, was designated to protect estuarine
systems (https://coast.noaa.gov/nerrs/; Voulgaris and Meyers
2004). Globally, marine protected areas such as these serve to
protect estuarine systems as well as monitor flora, fauna, and
water quality (http://www.mpatlas.org/; Washburn and Sanger
2011). While monitoring is critical for understanding changes
over time, methods utilized today have changed little over the
past decades. Likely due to their proximity to human population
centers, many estuaries have had the luxury of scientific
monitoring for decades including measurements of nutrients
and suspended sediment loads. These historic data provide
important baseline information for studying changes to
estuaries over time. The benefit is that multi-decadal stages are
being published examining ecosystems (e.g., Thronson and
Fig. 2 Oyster ground extent in US estuaries historically (a)andpresently(b). Note significant decline throughout US coastal and estuarine regions
regardless of latitude or coast (Zu Ermgassen et al. 2012, reprint of open access material)
Fig. 3 Percentage of estuary area containing oyster grounds historically and present by US coast line (Zu Ermgassen et al. 2012, reprint of open access
material)
Estuaries and Coasts
Quigg 2008;Paerletal.2014; Steichen and Quigg 2018)which
reveal the prevailing consequences of long-term land use chang-
es on water quality, including its degradation.
Given the high flux volumes and rapid transformations occur-
ring in estuaries worldwide, there is a pressing need to incorpo-
rate modern technologies and methods alongside traditional
monitoring to improve our understanding of estuaries and human
impacts on water quality and estuarine ecosystems. Here, several
direct impacts of urbanization on estuarine ecosystems and water
quality are discussed. The breadth of topics included is represen-
tative of the wide range of human impacts, many of which are
not immediately apparent to the individuals living in population
centers adjacent to the coast. Effects are potentially only perceiv-
able downstream or after a time delay, making it even more
important to understand adverse effects of human impacts and
urban development on our natural buffer zones so that preventa-
tive action and mitigation strategies can be enacted.
Sediment Dynamics in Tidal Creek Systems
Tidal creeks act as a gateway between uplands and marshes to
estuaries and coastal waters. These smaller water bodies are in-
fluenced by both freshwater flows running off the landscape and
continuous tidally driven changes in salinity (Holland and Sanger
2008). The upland areas of these watersheds are often popular
locations for development due to the adjacent coastal landscape.
These ecosystems are important habitat for commercial and rec-
reation fishes, including seatrout, crevalle jack, flounder, spade-
fish, spot, black drum, blue crab, brown shrimp, and white
shrimp (Hackney et al. 1976; Shenker and Dean 1979;Kneib
1997; Beck et al. 2001). Tidal creeks act as a gateway of sedi-
ments, nutrients, and water to and from adjacent wetlands. The
wetlands serve vital roles for ecosystems, act as niche habitats for
organisms, act as an initial “filter”of water from the landscape,
and provide coastal protection from storms through wave atten-
uation (Daborn et al. 1993; Goodwin et al. 2001;Graneketal.
2009; Townend et al. 2011; Shi et al. 2012;Mölleretal.2014).
The physical and biological dynamics of tidal creek and wetland
ecosystems are intricately connected. Changes that occur at that
landward (e.g., stormwater runoff, shoreline hardening, land
clearing) and seaward (e.g., trawling, sea level change) ends of
tidal systems may alter the resilience of these habitats in the
future. Rapid economic development and associated land use
change in these coastal areas can increase point and nonpoint
source pollution loading into these tidal creeks and nearby estu-
aries, influencing productivity, biodiversity, and ecological func-
tioning of these systems (Vitousek et al. 1997). Previous research
on tidal creek systems has focused primarily on freshwater dis-
charge, water quality, macrobenthic communities, and biodiver-
sity (Voulgaris and Meyers 2004; Corbett et al. 2007;Sanger
et al. 2008; Corbett et al. 2009; DiDonato et al. 2009;
Washburn and Sanger 2011; Gleeson et al. 2013; Webster et al.
2013; Sanger et al. 2015). There has been much less focus on the
response of sediment dynamics associated with land use change,
particularly development, in these critical coastal ecosystems.
Suspended sediment is cited as the most prolific water pollutant
(USEPA 2004,2006) and therefore studying sediment dynamics
within coastal tributaries and estuaries is critical to better manage-
ment. It is commonly found that sediments introduced to coastal
systems are chemically and physically bound with terrestrially
based nutrients and other sediment associated pollutants (e.g.,
heavy and trace-metals, herbicides, pesticides) and ultimate deg-
radation of these water bodies (Schropp et al. 1990; Riggs et al.
1991; Phillips 1997; Paerl et al. 1998;Hylandetal.2000; Buzzelli
et al. 2001;Paerl2006;). In shallow coastal tributaries and estuar-
ies, there is continuous exchange and deposition of particle-
reactive materials between the water column and bed sediment
(Giffin and Corbett 2003). Because of this, there is a need to study
the sediment dynamics of these urbanized estuarine systems if we
are to better understand their function as sediment sources or sinks,
as well as their sedimentological characteristics. However, only
focusing on the sediments does not provide insight into the drivers
that lead to the ultimate accumulation of material. Additional focus
on the biogeochemical transformations of the material along its
route to deposition/accumulation would better link the sediments
to the biological community and productivity. Other studies have
shown the impact of development in tidal creek watersheds to
detrimental changes in the benthic biological community
(Lerberg et al. 2000; Holland et al. 2004). Linking sediment deliv-
ery, quality, and dynamics to land use change and biological
diversity/productivity would be a next logical step in better man-
aging these systems.
Remote Sensing of Suspended Sediment
Concentrations
Estuaries have long been considered a “filter”for
suspended sediments and material bound to those sediments
such as pollutants and organic debris (Schubel and Carter
1984). Classically suspended sediment study was limited
case studies using water samples and cores. Satellite and
aerial imaging of waterways provides a means of rapidly
filling spatiotemporal gaps in traditional sampling of
suspended sediment concentration; however, it does so at
the cost of spatial resolution. Satellite-based instruments
image a particular scene on a daily to weekly timescale,
with a spatial resolution of 15–250 m. Studies combining
field data collection of water samples with remote sensing
imagery evaluation have found a high degree of accuracy
even in coarse spatial resolution (250 m) MODIS imagery
(Miller and McKee 2004). The broad spatial information
offered by remote sensing is critical for examining sediment
loads in estuarine systems as transport may occur on scales
of 1000s of kilometers (e.g., Van Rijn 1993;Miller
Estuaries and Coasts
and McKee 2004). Use of remotely sensed imagery also
allowed assessment of a large spatial scale on prolonged
time scales (20+ years) from historical records (e.g., Zhou
et al. 2017;Wangetal.2018).
Many studies have explored the relationship between re-
mote sensing reflectance at the sea surface from an atmospher-
ically corrected satellite image and suspended sediment con-
centration, as early as the 1980s (Stumpf and Pennock 1989).
There is an exponential relationship between these quantities,
particularly at mid-range sediment concentrations from about
10 to 30 mg/L (Freeman et al. 2017). A wide variety of algo-
rithms have been developed to link these two quantities using
in situ data alongside concurrently collected satellite or aerial
imagery. It is critical to carefully assess the conditions under
which an algorithm was developed prior to applying it to a
new imagery dataset. Many field-based algorithms are linear
and are most applicable to the conditions under which they
were developed, and will not perform well for regions with
much higher or lower concentrations of suspended sediment
(Freeman et al. 2017)(Fig.4). That said, there is immense
information contained in remotely sensed imagery for studies
of suspended sediment loads in estuarine systems, or related
material such as organic matter, chlorophyll, and pollutants
which bind to sediments. Studies combining in situ samples
with remotely sensed imagery provide the highest degree of
accuracy and spatial extent; however, enough ground work
has been laid to date to extrapolate meaningful information
about sediment concentration from satellite imagery for nearly
any estuarine system.
While earlier studies focused on validating relationships
between remote sensing reflectance and suspended sediment
concentration, the abundance and improved resolution of re-
motely sensed imagery has allowed for more detailed studies.
Mixing over distance is now being studied remotely and on a
larger scale thanks to Landsat imagery (Umar et al. 2018).
Interplay of different physical forcing from tides, waves, and
seasonal events such as monsoon are now being tied to sedi-
ment load with a high level of fidelity utilizing a combination
of geostationary and mobile platforms (Zhou et al. 2017).
Furthermore, remote sensing has opened a window to under-
stand variability of different physical influences (such as
freshwater inflow and wave events) on regions of clear and
turbid water in both shallow and deep water (Ruhl et al. 2001).
Established relationships tend to link one band (usually red or
infrared) of remote sensing reflectance to suspended sediment
concentration. Modest performance increase has been obtain-
ed using multi-band algorithms for scenarios where a higher
degree of accuracy may be necessary (DeLuca et al. 2018).
Harmful Algal Blooms—Insight from a South
African Case Studies
The increased global incidence of harmful algal bloom (HAB)
events is closely linked to the urbanization of coastal areas
resulting in intensification of anthropogenic nutrient loading
(Paerl and Scott 2010; Havens and Paerl 2015). The primary
concern arising from such HAB events is founded in the array
Fig. 4 Comparison of suspended particulate matter (SPM) measured in
situ from water samples in a variety of water types with calculated SPM
utilizing at surface reflectance from a handheld radiometer and a suite of
algorithms relating reflectance to sediment load. Note that there is
increased spread between calculated values at higher sediment
concentrations, and that each algorithm has a “niche range”in which it
performs well. (Freeman et al. 2017)
Estuaries and Coasts
of possible consequences. Some of these include oxygen de-
pletion related to bloom decay processes (i.e., respiration),
direct toxic effects on higher trophic levels (i.e., shellfish poi-
soning and bioaccumulation), mechanical interference and
suffocation of faunal communities (e.g., mucilage produc-
tion), and habitat destruction through shading of submerged
aquatic vegetation. Further complicating the issue of HABs
are the variety of mechanisms employed by species—both
microalgae and protozoans—which enable their proliferation.
Therefore, global issues, such as the accelerated distribution,
frequency, magnitude, and variety of HABs, “require the in-
terfacing of phenomena that occur on very different scales of
space, time and ecological organization”(Levin 1992).
The dynamics of HABs, and phytoplankton communities
in general, are controlled by both local processes and physical
transport processes (Qin and Shen 2017). A combination of
bottom-up (e.g., nutrient supply, light availability, tempera-
ture) and top-down (e.g., grazing pressure and interspecies
competition) controls constitute the local processes structuring
these communities. Alternatively, external transport processes
(e.g., tidal exchange, freshwater discharge and wind-driven
circulation) serve as the physical forces driving observed pat-
terns. Therefore, given the plasticity regarding the periodic
fluctuations for each of these processes (hourly, daily, season-
ally, annually, or stochastic), the relative importance of local
and external transport drivers varies with timescales. As such,
gaining an understanding of external and internal processes
governing spatio-temporal patterns of phytoplankton commu-
nities allows for natural progressions to be discerned from
anthropogenically induced change (Hall et al. 2015).
Detailed site-specific investigations of HABs are thus required
to explain the diversity of patterns at multiple temporal scales
and to understand the ecological significance thereof (Cloern
and Jassby 2010).
Given the significant economic and social development
opportunities provided by aquatic ecosystems, the prevention
of continued urbanization and expansion of catchment activ-
ities is unlikely (Satterthwaite et al. 2010), thus necessitating
an adaptive and proactive approach to conservation of these
ecosystems. Potential management options geared at restoring
a degree of natural phytoplankton functionality at an annual or
seasonal scale are primarily catchment based, while those
aimed at disrupting short-term processes can be implemented
at the catchment scale or in situ. The Zandvlei (Cape Town)
and Swartkops (Port Elizabeth) estuaries provide two South
African examples of where increased urbanization has culmi-
nated in eutrophic conditions and the proliferation of HABs.
The temporarily open/closed Zandvlei Estuary is subject to
numerous impacts associated with urbanization, including
catchment hardening (increased runoff), river canalization,
dredging, habitat loss, flow obstruction (weir and causeway
construction), and elevated nutrient inputs. The impacted na-
ture of the system, low salinity environments (< 10), and the
propensity for closed mouth conditions have facilitated peri-
odic HAB proliferations of Prymnesium parvum
(Prymnesiophyceae) since the 1970s (Whitfield et al. 2016).
In 2012, an extensive bloom of P. parvum significantly
discolored surface waters and resulted in oxygen depletion
and mass fish mortalities within the estuary. Subsequently,
an effective adaptive management approach geared at
preventing such incidents, together with continuous monitor-
ing, has been adopted by the local authorities. Current man-
agement interventions include submerged macrophyte har-
vesting (maintain nutrient uptake capacity), mouth manipula-
tion (increased salinity variability), and dredging (improved
connectivity).
Unlike the Zandvlei Estuary, management of the perma-
nently open and eutrophic Swartkops Estuary is more com-
plex given its size and multiplicity of anthropogenic activities
concentrated in the lower reaches of its catchment, including
industrial, wastewater treatment plants (WWTP), and
stormwater inputs (Scharler and Baird 2003; Lemley et al.
2017a). Of these, the WWTP inputs have the most notable
impacts, with the effects being twofold, i.e., consistent daily
inputs of freshwater and inorganic nutrients. Therefore, be-
cause the probability of reducing discharge rates from the
WWTPs is unlikely, due to the high demand placed on these
facilities, efforts should be focused on reducing the high N and
P loading. One way in which this can be achieved is through
the adoption of a dual-nutrient reduction approach to waste-
water treatment (Conley et al. 2009). Interestingly, the high
inorganic P levels in the Swartkops Estuary currently serve to
skew inorganic N:P molar ratios which in turn constrain the
magnitude of phytoplankton blooms through N-limitation. In
saying this, HABs of species belonging to the Peridinium
genus (Dinophyceae) have been documented to occur in the
stratified, occasionally hypoxic, upper reaches of the estuary
(Lemley et al. 2017a). Therefore, exacerbated eutrophication
symptoms (e.g., HABs) could be expected in the estuary by
only reducing P loads.
Thorough assessments of HAB dynamics in South
African estuaries have been largely understudied, with the
Sundays Estuary providing the only example in the literature
where this has been addressed. Linked to the urban demand
for agricultural products (Satterthwaite et al. 2010), acceler-
ated rates of urbanization are central to the expansion of
agricultural activities in the Sundays Estuary catchment. An
early study in the late 1980s (Hilmer and Bate 1991) was the
first to document the occurrence of two HAB species, name-
ly Heterocapsa rotundata (Dinophyceae) (formerly
Katodinium rotundatum)andHeterosigma akashiwo
(Raphidophyceae). As such, a recent review of microalgae
as indicators in South African estuaries (Lemley et al. 2016)
highlighted—among others—the need for (1) “hypothesis-
driven,”fine-scale experimental research, and (2) compre-
hensive autecological studies of HAB species. Geared at
Estuaries and Coasts
addressing these knowledge gaps, an intensive 3-year sam-
pling program was initiated in the Sundays Estuary. Annual
(Lemley et al. 2017a) and seasonal (Lemley et al. 2017b)
studies verified the persistently eutrophic condition of the
estuary and, more specifically, the progressive and recurrent
nature of extensive HABs of H. akashiwo and H. rotundata
(> 550 μg Chl-a/L) occurring in spring/summer and winter,
respectively. The Sundays Estuary provided an ideal ecosys-
tem to delve into the short-term processes (daily and hourly
studies) driving phytoplankton dynamics, due to its highly
regulated (interbasin water transfer scheme and irrigation ca-
nal network) and seasonal (temperature profiles, nutrient in-
puts and phytoplankton dynamics) nature. These investiga-
tions (Lemley et al. 2018a,b) identified seasonal bottom-
water hypoxia trends to be a direct consequence of collaps-
ing H. akashiwo spring/summer HABs. Additionally, inor-
ganic nutrient availability (nitrate and phosphate) was iden-
tified as the key bottom-up control promoting biomass accu-
mulation, while also limiting the magnitude and duration of
HAB events, while a vertically stratified water column con-
comitant with mesohaline surface waters (~ 10) were identi-
fied as conditions promoting the success of observed HAB
species (H. akashiwo,H. rotundata,Mesodinium rubrum,
and Karenia cf. mikimotoi). The significance of internal bi-
otic processes was revealed during the hourly investigation,
with the plasticity of diel vertical migration behavior, reli-
ance of M. rubrum on suitable cryptophyte “prey”resources,
and the allelopathic effects of H. akashiwo on co-occurring
taxa explaining phytoplankton community dynamics beyond
the influence of physicochemical variability. These findings
provided insight regarding the ecology of HAB taxa and
how they have adapted to thrive in anthropogenically manip-
ulated environments. As such, the broad- to fine-scale infor-
mation obtained for the Sundays Estuary (Fig. 5) offered the
opportunity to suggest management options specifically
geared at mitigating against the occurrence of HAB prolifer-
ations in similar ecosystems, including urbanized systems.
Potential management actions during HAB periods include
mechanical harvesting and algal flocculation techniques as a
means of biomass removal (Dai et al. 2015). However, many
HAB species are well-adapted to persisting during unfavor-
able conditions, e.g., alternating benthic-pelagic life histories
and mixotrophic capabilities. Therefore, the most feasible
approach regarding the management of HABs in estuaries
is to implement measures at the catchment scale (e.g., bene-
ficial management practices, recycling of wastewater, and
scheduled dam releases). These will serve to increase the
incidence of episodic disturbances and reduce the extent of
press disturbances, with the ultimate objective of (1) main-
taining a state of flux in the phytoplankton community, (2)
limiting the frequency and magnitude of HAB events, and
(3) disrupting the seasonal nature of bottom-water hypoxia
(Fig. 6).
The persistent occurrence of harmful phytoplankton taxa is
a new feature in South African estuaries, and as such further
research is required to assess the distribution, magnitude, va-
riety, and ecology thereof. However, given the logistical con-
straints associated with many developing regions, including
South Africa, there are numerous research gaps which need to
be addressed to facilitate effective management of HABs,
some of which include:
1. Identification of alternative resource pools (i.e., organic
nutrients and bacterial communities) that facilitate the per-
sistence and dominance of HAB species.
2. Microcosm experiments aimed at isolating the effect of
specific environmental variables on HAB species to make
predictions regarding global change scenarios.
3. Assessment of how primary consumer communities (e.g.,
copepods and larval fishes) respond during HAB periods.
4. Molecular comparisons with global strains of HAB spe-
cies to elucidate the potential dispersal mechanisms facil-
itating their global occurrence.
5. Feasibility studies of remote sensing as a tool with which
to monitor estuarine HABs.
6. Installation and implementation of continuous in situ
HAB monitoring technologies.
Pathogen Accumulation in Shellfish Due
to Urbanization Near Estuarine Watersheds
Human illness associated with bacterial pathogens has risen
alongside population density growth in major cities (i.e., New
York City) since the late nineteenth century. This time period
corresponds with the initial construction of sewage systems in
many urban areas, which delivered human wastes to the nearby
estuaries (Rippey 1994). Since then, over 400 different out-
breaks have been reported, many of these due to bacteria in
wastewater (Rippey 1994). The National Shellfish Sanitation
Program and sanitation surveys created in the 1920s (to track
effluent and point source inputs) helped to reduce the number
of human illnesses (DePaola et al. 2010). Coastal urbanization
can lead to elevated inputs of enteric bacteria (fecal coliforms)
and nutrient rich waters over subtidal/intertidal shellfish beds,
including commercially and ecologically important areas of
clams, scallops, and oysters (Mallin et al. 2000; Campos and
Cachola 2007; Maalouf et al. 2010;Camposetal.2013). Many
of these organisms live in small estuaries and creeks
surrounded by impervious surfaces and agricultural land, and
shellfish beds can be closed due increasing fecal coliform bac-
terial concentrations (Mallin et al. 2000). For example, in the
New Hanover County watersheds, NC, there are five tidal
creeks with 42.9–77.8% developed land, and in the low
Estuaries and Coasts
salinity regions of the creeks, all five had elevated fecal
coliform counts over a sampling season.
EPA standards for shellfish sanitation and shell fishing
(1986) indicate that regular fecal coliform sampling should
occur to adequately monitor conditions in the water column
that could impact the oysters on the bottom (Campos et al.
2013). If routine sampling shows a medial fecal coliform con-
centration above 14MPN/100 mL (or 10% above 43MPN/
100 mL), then water is not safe for shellfish harvesting (EPA
Water Quality Criteria 1986). The concentration of fecal indi-
cator organisms that are in the water column serve as a good
indicator of what is in the shellfish meat; however, multiple
environmental and physiological factors influence the accu-
mulation of fecal coliforms within oyster tissue (reviewed in
Campos et al. 2013). Historically, most outbreaks of bacterial
pathogens occur in the summer months (Rippey 1994). A
nationwide survey of marketed oysters in 2006 examined mi-
crobial indicators in shellfish (along with other viral patho-
gens) and found that mean levels of fecal coliforms and
E. coli during summer were above the FDA limits for con-
sumption in some regions (DePaola et al. 2010); in areas with
closed shellfish beds, illegally harvested oysters could have
much higher pathogen loads and cause illness when consumed
(DePaola et al. 2010). Maalouf et al. (2010) examined histor-
ical data looking at illness outbreaks associated with sewage
discharges over shellfish beds, and found many linkages be-
tween the two. Outbreaks of gastroenteritis due to fecal coli-
formsinsewageeffluentwerelinkedtocontaminatedoysters
in Australia, New York, and France in the past three decades
(Maalouf et al. 2010).
The amount of urbanization in the surrounding watershed
can be estimated by the degree of impervious surfaces sound-
ing the waterways. Impervious surfaces mean that during pe-
riods of high rainfall, any pollutants on the surfaces wash into
the storm drains/creeks. Mallin et al. (2000) found that if
creeks were surrounded by greater than 10% impervious sur-
faces, they were periodically closed to shell fishing activities
due to increased fecal coliform bacteria. Comparison of the
fecal coliform abundance with the percentage of impervious
surface showed a strong correlation (Pearson correlation r=
0.975, p< 0.005). Impervious surfaces mean that during pe-
riods of high rainfall, any pollutants on the surfaces would
wash into the storm drains/creeks. During a thorough sam-
pling season highlighting various rainfall amounts,
Coulliette and Noble (2008) saw a significant relationship
between the quantity of rain and the quantity of fecal coliform
Fig. 5 Sundays Estuary region
discussed in the harmful algal
bloom South Africa case study
Estuaries and Coasts
bacteria (E. coli and Enterococcus) in the water columns of the
Newport River Estuary (NC, USA). Not only did rainfall
(above the recommended threshold for shellfish sanitation
safety) cause E. coli and Enterococcus levels to rise above
the regulated MPN/100 mL levels, there was also a significant
rise in fecal indicator bacteria during dry periods, possibly due
to a reservoir of cells in the sediment that were suspended into
the water column due to human activity in the creeks (Fig. 7).
Input of pathogenic bacteria into an enclosed waterway
(i.e., a tidal creek) can impact not only the water column but
the sediments as well. Fecal coliform bacteria can be deposit-
ed onto the substrate during sedimentation, adding to the sed-
iment microflora. It is highly likely that they would be resus-
pended during tidal cycles, or human interactions (wading in
the creek, swimming, etc.). Following a raw sewage spill,
Mallin et al. (2007) found that sediment bacteria counts
Fig. 6 Summary of the processes facilitating the proliferation and recurrent nature of two commonly occurring harmful algal bloom species in the
Sundays Estuary (note: the factors promoting and limiting the growth of these two species are indicated in green and red text, respectively)
Estuaries and Coasts
remained elevated for weeks, and increased yet again follow-
ing an intense precipitation event (Mallin et al. 2007). Once
resuspended, fecal coliform bacteria that were present in the
sediments (i.e., 200 CFU/cm
2
) showed corresponding quanti-
ties in the water column (i.e., 200 CFU/100 mL). Since sedi-
ments can accumulate viable bacterial cells rapidly (acting as a
reservoir for cells), this could cause a rapid increase in water
column bacteria concentrations above the recommended
threshold for human contact (Al Aukidy and Verlicchi 2017;
Madoux-Humery et al. 2015; Coulliette and Noble 2008;
Mallin et al. 2007). Stormwater input can cause increased
turbidity as well, due to both the input of particulates in the
runoff as well as the resuspension of existing sediments
(Coulliette and Noble 2008). Several studies in both
subtropical and temperate regions have demonstrated the
survival of fecal indicator bacteria in the sediments;
Coulliette and Noble (2008) linked periods of increased fecal
indicator bacteria even during dry times to this ‘reservoir ef-
fect’(Fig. 7).
Urbanization-Driven Land Use Changes:
Galveston Bay Case Study
The conversion of land to support growing populations is a
major component of human modification of the environment
around the world (Alberti et al. 2003; Alberti 2005;Diazand
Rosenberg 2008; Paerl et al. 2014). An examination of land
use land cover data is an important element in helping us to
understand the environmental and anthropogenic influences
affecting waterways and watersheds (Carle et al. 2005;Lee
et al. 2009). Urbanization, industrialization, agriculture,
deforestation, loss of wetlands, and several other types of land
use change have taken place in response to human population
growth in watersheds all over the world. Urban-related runoff/
stormwater is one of the largest contributors to the impairment
of river and stream water quality in most US states (USEPA
2010; Paerl et al. 2014), with high levels of eutrophication
reported in 45% of the estuaries surrounding the Gulf of
Mexico (Clement et al. 2001).
Recent efforts to understand water quality degradation
have focused on the watershed of Galveston Bay (TX), a
subtropical estuary in the north-western Gulf of Mexico
(Fig. 8). With a billion-dollar commercial and recreational
fishery, home to the US energy nexus, several large ports
and cities, the Galveston Bay ecosystem is under pressure
from a variety of sources (Lester et al. 2013). Yet unlike
Chesapeake Bay and San Francisco Bay (see e.g., Dauer
et al. 2000; Smith et al. 2003;Kempetal.2005;Glibert
et al. 2011), clear effects of the environmental pressures asso-
ciated with eutrophication or invasive species have not yet
been observed in Galveston Bay (Gonzalez and Lester 2011;
Steichen et al. 2012,2015). Ongoing efforts are focused on
understanding the tipping points in this estuarine system (e.g.,
Roelke et al. 2013;Doradoetal.2015;Pinckneyetal.2017).
The Galveston Bay watershed (72,000 km
2
)includes
Houston and Dallas, ranked as the fourth and ninth largest
cities and fastest growing cities in the USA, respectively
(Census 2012, https://www.census.gov). Further, the cities of
Austin and Fort Worth rank eleventh and sixteenth, so it is not
surprising that the population density in Texas is expected to
double by 2050 (Texas Water Development Board TWDB
2007). Galveston Bay (1554 km
2
), at the southern end of the
watershed, is the second largest estuary in the Gulf of Mexico.
Fig. 7 aFecal coliform (FC) concentrations found in the Newport River
Estuary, NC, according to general rainfall categories of < 0.25 cm, 0.25–
2.54 cm, > 2.54 cm, and then in regard to the management action plan of
< 3.81 cm and > 3.81 cm. The dotted line indicates the FC standard limit
of 14 MPN per 100 ml. Asterisks indicate a significant difference as
compared to other categories. Error bars indicate ±1 standard error. b
Mean FIB concentrations at Newport River Estuary sampling sites
categorized by distance from land (close≤0.25 km to shoreline,
distant ≥0.25 km to shoreline). Error bars indicate ± 1 standard error.
Reproduced from Journal of Water and Health Volume 6, issue number
4, page 478, with permission from copyright holders IWA Publishing
(Coulliette and Noble 2008)
Estuaries and Coasts
It has two major rivers flowing into its northwest (San Jacinto)
and northeastern (Trinity) reaches. These rivers bring in 16
and 55% of annual freshwater inflows (Guthrie et al. 2012)
into the Bay. While the San Jacinto River flows through the
highly urbanized and industrialized Houston, the Trinity River
is surround primarily by forested and grassland areas imme-
diately north of the Bay (H-GAC 2017).
An examination of land use change maps (National
Land Cover Data) between 1996 and 2011 classified
by H-GAC using the NOAA Coastal Ocean
Program’s Coastal Change Analysis Program (C-
CAP) (see H-GAC 2017) indicate an 11% increase
in area used for development in Harris County (were
Houston is located) since 1996 (Fig. 9). An exami-
nation of all the counties surrounding Galveston Bay
revealed that forest land cover experienced the
greatest loss, primarily due to development
(urbanization) during this period (Fig. 9). Forests
were also lost to grasslands and more shrubs as well
as losses to agricultural (cultivated) lands and wet-
lands (Fig. 9). In most cases, wetlands were convert-
ed into developed lands, to shrubs and grasslands
associated with urban community centers, particularly
those connected to waterways (Figs. 8and 9; H-GAC
2017).
As a result of the Clean Water Act and other pol-
icies, nutrient and chlorophyll a (often used as a
proxy for phytoplankton biomass) levels have been
declining in Galveston Bay since the 1970s, although
less so in more recent years (Gonzalez and Lester
2011). This decline and/or change may also be the
result of less agricultural lands surrounding the bay.
The losses of wetlands likely preceded the period of
record for the land use/land change maps.
Nonetheless, we know that consequences of these
losses include both habitat quality and dietary chang-
es that impact higher trophic levels. One of the larg-
est increases associated with development in the
Fig. 8 The Galveston Bay watershed extends from Dallas/Fort Worth to
Houston to Galveston Island (see inset). Counties surrounding Galveston
Bay in the lower watershed and nearby are: Matagorda, Brazoria,
Galveston, Chambers, Liberty, Harris, Fort Bend, Wharton, Colorado,
Waller, Montgomery, Waller, and Walker. The majority of freshwater
inflows (~ 81%) enter from the Trinity and San Jacinto Rivers, and
Buffalo Bayou (not shown)
Estuaries and Coasts
Galveston Bay watershed has been waterways, either
as detention ponds and lakes or canalization associat-
ed with residential developments (H-GAC 2017).
These are known to be localized zones of degraded
water quality, particularly canals that often have a
dead end, and experience increased hypoxia and/or
harmful algal blooms, predominantly in warmer
months (Gonzalez and Lester 2011). Galveston Bay
was found to be a hotspot for fish kills over a
multi-decadal period (Thronson and Quigg 2008).
Despite this, overall fish abundance and diversity
has not changed significantly (Steichen and Quigg
2018).
It hypothesized that until now, GalvestonBay has been resilient
to the upstream changes in land use and land cover, in terms of
eutrophication and subsequent hypoxia and invasive species. The
former has not yet been measured, and little information is avail-
able to confirm the latter. The lack of obvious signs of eutrophica-
tion may in part be facilitated by the relatively high freshwater
inflows and short turnover time in the bay (Roelke et al. 2013;
Dorado et al. 2015). This may also be due to the fact that the vast
majority of developed lands (as urbanization) flushing into the
river contributes to only one sixth of the bays freshwater inflows;
the other important river (Trinity) contributes more than half the
freshwater inflows but has had fewer alterations to its landscape,
which is primarily forest and wetlands areas. It may also be that the
watershed as a whole has not been overdeveloped, that is, water-
sheds with ≥10% altered land hit the threshold for water quality
decreases due to impervious surface effects (Walsh et al. 2005;
Zampella et al. 2007). Nonetheless, as regional planning and
natural resource management endeavors to determine the appro-
priate amount of freshwater inflows for Galveston Bay, under-
standing the balance between land use land cover change andwater
quality will be key to maintaining ecosystem services and func-
tions for future generations. This is challenging as linear responses
to land use change are unlikely given the complex and dynamic
nature of estuarine systems.
Hurricane Harvey made landfall from August 25–30 (2017)
and set a continental US record for rainfall with more than
100 cm in this short time frame (van Oldenborgh et al. 2017;
Emanuel 2017). The massive flooding in urbanized areas is
thought to be a result of prolonged changes in land use including
development in low lying areas and flood plains along with
deferred maintenance projects which results in a weakening of
protective barriers around major bayous. Along with extensive
flooding, overflowing reservoirs, and overtopping dams, >
100,000 homes were damaged along with numerous schools
and businesses (Shultz and Galea 2017). Of the more than 13
million persons directly affected by the storm, 6.5 million were
impacted by the rainfall (NOAA NCEI 2017). Highly contami-
nated Superfund sites in the Houston area were deluged by flood-
waters; these along with spills from inundated sewage and waste-
water systems released > 31 million gallons of raw sewage
(Stuckey 2017). Pollutants released by Texas facilities into
Galveston Bay include benzene, 1,3-butadiene, hexane, hydro-
gen sulfide, toluene, and xylene, at least two of which are cancer-
causing chemicals and > 700,000 pounds of sulfur dioxide,
which can lead to the formation of dangerous contaminants
(FEMA 2017). The impact on the health of the bay is the source
of many ongoing studies. While the flood waters effectively
Fig. 9 The percentage change in land use in counties surrounding
Galveston Bay (see Fig. 8). In Harris, Fort Bend, and Montgomery
counties, the grow corridor of Houston and surrounding areas, there
was a significant increase in developed lands. As a result, there was a
significant decrease in forested lands in Harris and Montgomery counties
while agricultural lands were lost in Fort Bend county. Development also
impacted the land cover in Galveston, Brazoria, Liberty, and Chambers,
but to a lesser extent. Loss of forested land was significantly in Liberty;
this coincided with increase in grass cover
Estuaries and Coasts
“flushed”out the bay, and possibly associated nutrients and pol-
lutants, the concurrent scouring of the sediment bottom, particu-
larly in the industrial areas around Houston and its ship channel
may have (re)introduced legacy contaminants such as dioxins,
PCBs, lead and others (this data is however not yet published).
Ongoing studies will be required to monitor how this massive
disruption on urban systems negatively impacts the health of
Galveston Bay.
Environmental Limits of Ecosystems: Oyster
Case Study
Urbanization has affected coastal species composition and eco-
system function in part by changing biogeochemical processes
within the water column (Levin et al. 2014). These alterations
can ultimately reduce the survival of species, particularly for
those already nearing their physiological tolerance limits. One
keystone species found throughout urbanized estuaries along
the US East Coast and Gulf of Mexico is the eastern oyster
Crassostrea virginica.C. virginica possesses a complex life
cycle that includes a benthic adult stage and a pelagic larval
phase (Fig. 10). While C. virginica adults are relatively robust
to the dynamic physical conditions observed in coastal waters
(Bauman et al. 2015), reproduction and survival of early life
stages may be disproportionately negatively affected by urban-
ization. Though factors such as pollution, sedimentation, and
competition predation by invasive species have been shown to
hurt oyster populations, here the focus is on urbanization-
driven changes in physical parameters. Specifically, the effects
of eutrophication-driven hypoxia, eutrophication-driven hyper-
capnia, and lowered salinities from altered streamflow on sur-
vival of C. virginica are explored.
As mentioned in previous sections, one component of ur-
banization, increased area of impermeable surfaces and sub-
sequent runoff, raises the supply of limiting nutrients to coast-
al waters, leading to phytoplankton blooms. These blooms are
critical to successful fisheries. However, the subsequent
bloom die-off and respiration of organic matter produces pe-
riods of hypoxia, which may be pronounced in areas of high
stratification (Baker and Mann 1992). While adult oysters can
withstand prolonged hypoxic periods of days to weeks
(Stickle et al. 1989), hypoxia and anoxia reduce both larval
set and spat survival in C. virginica (Baker and Mann 1992).
In shallow eutrophic tributaries, diel cycling hypoxia is com-
monly observed during summertime, yet urbanization in-
creases the frequency and severity of the cycling (Keppel
et al. 2015). Although normoxic conditions return daily, diel
cycling hypoxia both reduces feeding, and increases suscepti-
bility of eastern oysters to the protistan parasite Perkinsus
marinus. This potentially leads to estuarine-scale effects of
disease acquisition in the species (Breitburg et al. 2015;
Keppel et al. 2015). A recent study by Steppe et al. (in prep)
demonstrated that severe cycling hypoxia representative of
urbanization-impacted estuaries also affects oyster reproduc-
tion, both reducing the proportion of reproductive oysters
Fig. 10 Crassostrea virginica reproduction sampling locations. Circles indicate spat collector deployments; squares, reef collections; and stars,
continuous water quality sondes
Estuaries and Coasts
within a sample and lowering gonadosomatic index (the ratio
of the germinal tissue to visceral mass). Therefore,
eutrophication-driven hypoxia is detrimental to C. virginica
throughout its life cycle.
Eutrophication, often a result of urbanization and land use
changes, can also lead to the hypercapnic conditions that are
frequently found in coastal waters (Cai et al. 2011, Nixon et al.
2015;Baumanetal.2015). Reduced pH may inhibit
C. virginica shell formation (Waldbusser et al. 2010) and dis-
solve oyster shell base, reducing substrate available for spat
set (Waldbusser et al. 2011a, b). Sustained seasonal acidifica-
tion in line with predictions of severe climate change scenarios
has been shown to reduce reproductive success in C. virginica
by limiting oogenesis (Boulais et al. 2017). Likewise, constant
moderate pH (7.45) has been shown to reduce gametogenesis
in C. virginica (Steppe et al. 2019). These values (7.45) coin-
cide with values observed in early summer in Chesapeake Bay
tributaries (Steppe and Wallendorf 2017). Cycling pH, on the
other hand, does not affect oyster reproduction or disease ac-
quisition (Keppel et al. 2015, though it is associated with
increased hemocyte activity, a sign of physiological stress.
Urbanized coastlines have fundamentally changed the
physical and chemical parameters of estuaries. Along with
reduced oxygen and pH, sharply lowered salinities, such as
those caused by coastal storms and dam releases may hurt
oyster populations, particularly when these events coincide
with gametogenesis and larval development (Butler 1949).
Low salinities may reduce the buffering capability of estu-
arine water. Combined with hypercapnic conditions, this
mayreducelipidandglycogenstores,andincreasefractur-
ing of juvenile oyster shells (Dickinson et al. 2012).
Because mesohaline tributaries are often selected for oyster
restoration, due to reduced disease prevalence in these
areas (Westby et al. 2015), oysters may already be living
close to their salinity tolerance limits. Salinities below 6
may limit gametogenesis (Butler 1949), yet even when ga-
metogenesis is documented, spat recruitment, and subse-
quent growth is often low in these areas (Bergquist et al.
2006; Steppe and Wallendorf 2017). An example of this has
been observed in the Severn River, a mesohaline tributary
of Chesapeake Bay, Maryland USA, near the urban centers
of Baltimore, Annapolis, and Washington, DC. From 2011
to 2013, high-frequency water quality data (period =
15 min) were collected at multiple sites that coincided with
bi-weekly samples of oyster gametogenesis and spat.
Gametogenesis was observed each year of the study at three
reefs and in oyster grow-out cages, yet of 2760 oyster shell
valve “spat collectors”analyzed for recruitment, only 3
spat were recorded. The spat collected were all found in
2012, the only year of the three in which salinities remained
above the threshold of 6 throughout the entire spawning
period (Steppe et al. 2018).
In addition to spring freshets, salinities may fall due to
altered streamflow that cause prolonged periods of low salin-
ity. This includes dam and spillway releases that result from
severe storms (Turner 2006; LaPeyre et al. 2016). In 2011, the
Conowingo Dam was released in early September, as a result
of Hurricane Irene. The release caused the salinity to drop
from 9 to 2 at the Severn River study site, likely killing any
larvae that may have been in the water column at that time.
Similarly, a salinity drop from 8 to 3 in mid-July 2013 may
have led to increased larval mortality, and reduced recruitment
that year (Steppe et al. 2018).
Further research on the effects of urbanization on
ecosystems must be conducted to better understand the
role of anthropogenic stresses on water quality and eco-
system function. In particular, high-frequency observa-
tions of coastal physical parameters should be colocated
with biological sampling of species at each segment of
their life history. Additionally, results should be con-
veyed to managers to better time decisions (such as
dam releases) to coincide with period that are less
stressful to keystone species.
Closing Remarks
As human populations increase, and technology allows
further coastal development, there is a pressing need for
improved tools and data collection methods to rapidly
obtain meaningful data on broad spatiotemporal scales.
Human populations have been experiencing rapid
growth over the past century, in addition to a migration
towards the coasts. The rapidly changing landscape has
altered the nature of estuarine ecosystems and water
quality. In general, urbanization land use changes result
in increased runoff containing a higher concentration of
pollutants, nutrients, and toxic materials, which are in-
troduced to estuarine systems (Carle et al. 2005;
DiDonato et al. 2009). Many estuaries are now beyond
their capacity to synthesize or process these inputs,
meaning that the same pollutants, excess nutrient loads,
and toxic materials make their way downstream to the
oceans. The dynamics of suspended sediments, nutri-
ents, and pollutants, effects on shellfish, harmful algal
blooms, and impacts of land use changes, all have wide
reaching effects on estuaries around the world. The re-
ality is that while estuaries provide valuable ecosystem
services including seafood, recreation, and a buffer zone
from storm energy, urbanization and human develop-
ment are putting many of these important systems at
risk. It is our responsibility to understand the risks and
impacts, and make the best use of emerging technolo-
gies and data to mitigate and reduce the adverse conse-
quences for estuaries.
Estuaries and Coasts
Acknowledgments The authors are grateful to the participants of CERF
2017 Session 1299: Ruth Carmichael, Nelle D’Aversa, Bethany
DeCourten, Naomi Detenbeck, Brooke Frohloff, Alexandria Hounshell,
Michael T. Lee, Haley Nicholson, and Guangming Zheng, as well as the
organizers of the CERF 2017 Biennial Conference in Providence, RI.
LAF appreciates feedback and support from Art Miller & Simon
Freeman. AMF is grateful for released-time support from NJCU-
College of Arts & Sciences. AQ: the Houston-Galveston Area Council
graciously provided the land use land cover data (http://www.h-gac.com/;
December 2016). Without this data and support from the Galveston Bay
Estuary Program, this work would not have been possible. CNS thanks
USACE, Baltimore District, D. Brietburg, R. Burrell, (Smithsonian
Environmental Research Center) A. Keppel, and L. Wallendorf (United
States Naval Academy). An anonymous reviewer provided constructive
suggestions that greatly improved the quality of this manuscript.
Funding Information DRC is supported by the NC Sea Grant
(R/MG-1522). DAL is supported by the South African Network
for Coastal and Oceanic Research (SANCOR) and the National
Research Foundation (NRF) of South Africa through a postdoctoral
fellowship (grant number 112650)
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