An - Extreme - Future - For - Estuaries - Effects - Wetz 2013

Marine Pollution Bulletin 69 (2013) 7–18
Contents lists available at SciVerse ScienceDirect
Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul
Review
An ‘extreme’ future for estuaries? Effects of extreme climatic events

on estuarine water quality and ecology
Michael S. Wetz a,⇑, David W. Yoskowitz b
a
Department of Life Sciences, Texas A&M University-Corpus Christi, 6300 Ocean Dr., Unit 5892, Corpus Christi, TX 78412, United States
b
Harte Research Institute for Gulf of Mexico Studies, Texas A&M University-Corpus Christi, 6300 Ocean Dr., Corpus Christi, TX 78412, United States
a r t i c l e i n f o a b s t r a c t
Keywords: Recent climate observations suggest that extreme climatic events (ECE; droughts, floods, tropical
Estuary cyclones, heat waves) have increased in frequency and/or intensity in certain world regions, consistent
Water quality with climate model projections that account for man’s influence on the global climate system. A synthesis
Climate change of existing literature is presented and shows that ECE affect estuarine water quality by altering: (1) the
Tropical cyclone
delivery and processing of nutrients and organic matter, (2) physical–chemical properties of estuaries,
Drought
Flood
and (3) ecosystem structure and function. From the standpoint of estuarine scientists and resource man-
Fisheries agers, a major scientific challenge will be to project the estuarine response to ECE that will co-occur with
other important environmental changes (i.e., natural climate variability, global warming, sea level rise,
eutrophication), as this will affect the provisioning of important ecosystem services provided by
estuaries.
Ó 2013 Elsevier Ltd. All rights reserved.
Contents
1. Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
2. Effects of extreme climatic events on estuarine water quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
2.1. How do ECE affect estuarine water quality, and does this depend on the characteristics of a particular event?. . . . . . . . . . . . . . . . . . . . . . 8
2.1.1. Tropical cyclones and floods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
2.1.2. Drought . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
2.1.3. Interactions between droughts and tropical cyclones/floods. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2.1.4. Heat waves . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2.1.5. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2.2. How long do the effects of ECE persist, and how does this depend on the tidal regime of affected estuaries? . . . . . . . . . . . . . . . . . . . . . . 12
2.2.1. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
2.3. Is there a relationship between land-use coverage in estuarine watersheds and ECE-induced water quality changes? . . . . . . . . . . . . . . . 12
2.3.1. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
3. An extreme future for estuaries? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
3.1. Effects of more intense tropical cyclones and floods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
3.2. Effects of intensified and/or more frequent low freshwater inflow events . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
4. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
⇑ Corresponding author. Tel.: +1 361 825 2132; fax: +1 361 825 2025.
E-mail addresses: [email protected] (M.S. Wetz), david.yoskowitz@
tamucc.edu (D.W. Yoskowitz).
0025-326X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.marpolbul.2013.01.020
8 M.S. Wetz, D.W. Yoskowitz / Marine Pollution Bulletin 69 (2013) 7–18
ecological effects of ECE on the coastal zone, our knowledge is lim-

ited in terms of mechanistic linkages between particular events
and subsequent estuarine water quality and ecosystem responses.
This, in turn, hinders the ability of scientists and resource manag-
ers to project the trajectory and magnitude of future water quality
changes in estuaries and thus effectively manage these vital aqua-
tic resources. Here we summarize the effects of ECE on estuarine
water quality and important ecosystem services. We follow a con-
ceptual model that examines effects of ECE on external chemical–
biological loading to estuaries as well as effects on estuarine phys-
ical dynamics. We then document subsequent impacts on water
quality indicators and highlight the cumulative effects of these
changes on estuarine ecosystem health, goods and services (espe-
cially fisheries), all while attempting to identify important modu-
lating factors (Fig. 1). The emphasis will be on tropical cyclones,
floods, drought, and heat waves. We focus on the following
questions:
1. How do ECE affect estuarine water quality, and does this

depend on the characteristics of a particular event (e.g. timing,
duration, trajectory in the case of tropical cyclones)?
2. How long do the water quality changes caused by ECE persist,
and does this depend on the tidal regime of affected estuaries?
3. Is there a relationship between land-use coverage in estuarine
watersheds and ECE-induced water quality changes?
These questions must be answered to effectively project and

plan for the effects of future changes in frequency or intensity of
ECE and the eventual impacts on the provisioning of ecosystem
services.
2. Effects of extreme climatic events on estuarine water quality
2.1. How do ECE affect estuarine water quality, and does this depend
on the characteristics of a particular event?
2.1.1. Tropical cyclones and floods

Tropical cyclones (e.g., Paerl et al., 1998, 2001; Williams et al.,
2008) and floods (Wong et al., 2010) can mobilize significant quan-
Fig. 1. Schematic representation of the effects of extreme climatic events and tities of organic matter and suspended solids which are subse-
potential modulating factors (in italics).
quently deposited in estuaries. The combination of high organic
matter loads and stratification caused by the freshwater input
1. Background can interact to promote hypoxia/anoxia in subpycnocline water
and occasionally in the whole water column (Paerl et al., 1998;
Estuaries represent one of the world’s most vital aquatic re- Mallin et al., 2002; Burkholder et al., 2004; Tomasko et al., 2006).
sources, providing food resources and habitat for ecologically and In some cases, freshwater itself may contain relatively low (i.e.,
economically important fish and shellfish species, recreational hypoxic) oxygen levels that exacerbate these conditions (e.g.,
opportunities, scientific and educational experiences, and other Mallin et al., 2002; Tomasko et al., 2006). For example, Hurricanes
important ecosystem services (Costanza et al., 1997; Hobbie, Fran (Cat. 3) and Bertha (Cat. 2) caused abrupt, adverse changes in
2000; Pendleton, 2008; Yoskowitz et al., 2010). But estuaries the water quality of freshwater and estuarine ecosystems along the
worldwide are being exposed to an increasingly complex suite of US Atlantic coast in 1996. Runoff generated by these storms deliv-
environmental perturbations originating in their watersheds (e.g., ered considerable amounts of terrestrial organic matter, nitrogen
anthropogenic nutrient loading, land use change, hydrologic mod- (N)-rich organic matter from wastewater treatment facilities, and
ification) and externally from climatic forcings (e.g., tropical cy- inorganic nutrients into North Carolina’s Cape Fear River (Mallin
clones, droughts, global warming, sea level rise). The cumulative et al., 1999). This led to hypoxia/anoxia that persisted for nearly
effect(s) of these perturbations often includes declining water 1 month (Mallin et al., 1999, 2002). Large fish kills were reported
quality (eutrophication) and deleterious changes in ecosystem in the river, and further downstream in the Cape Fear estuary, hyp-
structure and trophic dynamics in many estuaries (Cloern, 2001; oxic conditions lasted several weeks and had deleterious effects on
Paerl et al., 2006; Rabalais et al., 2009). This, in turn, may alter or the benthic invertebrate community (Mallin et al., 1999, 2002). In
compromise the quantity and quality of goods and services pro- the nearby Neuse River Estuary, runoff from Fran delivered a large
vided by estuaries. volume of low oxygen, organic matter-rich freshwater to the sys-
Climate variability, and specifically extreme climatic events tem, also resulting in development of hypoxic/anoxic conditions
(ECE), strongly influences the delivery of freshwater and associated and fish mortalities (Paerl et al., 1998).
nutrients and organic matter to the coastal zone (Scavia et al., Tropical cyclones (Bales, 2003; Peierls et al., 2003; Burkholder
2002; Paerl et al., 2006). Despite evidence highlighting large-scale et al., 2004) and floods (e.g., Magnien et al., 1992; Hickel et al.,
M.S. Wetz, D.W. Yoskowitz / Marine Pollution Bulletin 69 (2013) 7–18 9
events, can create conditions that are unfavorable for phytoplank-

ton growth. Several studies have noted reductions in phytoplank-
ton productivity in estuaries immediately following tropical
cyclones (e.g., Paerl et al., 1998; Mallin et al., 2002) and floods
(Eyre and Ferguson, 2006; Murrell et al., 2007) due to reduced light
availability or excessive flushing. Certain taxa of phytoplankton do
appear to be favored under post-cyclone or flood conditions (i.e.,
relatively low light, high nutrient and organic matter concentra-
tions), including harmful species belonging to the Raphidophyceae
and Dinophyceae (e.g., Kempton et al., 2008; Hall et al., 2008). Be-
cause of the mixotrophic capabilities of many of these organisms,
they are capable of supplementing energetic demands under low
light conditions through utilization of organic matter and can thus
outcompete other phytoplankton such as diatoms and flagellates
(Burkholder et al., 2008; Jeong, 2011). When light limitation is
not a factor, tropical cyclones may rapidly (<1 week after passage)
stimulate phytoplankton productivity and bloom development as a
result of wind-driven resuspension of nutrients (e.g., Miller et al.,
2006; Wetz and Paerl, 2008). Phytoplankton blooms have also been
noted to occur after a lag phase of weeks to months post-cyclone or
flood (Paerl et al., 2001; Peierls et al., 2003; Eyre and Ferguson,
2006; Hagy et al., 2006; Murrell et al., 2007; Cook et al., 2010;
Voynova and Sharp, 2012), which allows ample time for the light
environment to become favorable again and flushing to lessen.
Seagrasses can also be affected by changes in the light environ-
ment that often accompanies tropical cyclones and floods. Light
stress caused by these events can lead to massive seagrass die-
off if low light conditions persist for many weeks to months (e.g.,
Preen et al., 1995; Longstaff and Dennison, 1999; Campbell and
Mckenzie, 2004; Carlson et al., 2010; Fig. 2). In contrast, shorter-
lived events tend to have minimal impact on seagrasses (e.g.,
Longstaff and Dennison, 1999; Anton et al., 2009). Furthermore,
seagrasses appear to be fairly resilient to the extreme physical
stresses caused by tropical cyclones (Steward et al., 2006; Anton
et al., 2009; Carlson et al., 2010), and several authors have noted
that these events may actually lead to seagrass range expansion
by dispersal of seeds (Kendall et al., 2004; Bell et al., 2008).
There is no question that tropical cyclones and floods can affect
estuarine water quality, but interestingly the degree to which this
occurs may be dependent on the characteristics of a particular
event (e.g., Mallin and Corbett, 2006; Wetz and Paerl, 2008;
Briceno and Boyer, 2010). For instance, it has been proposed that
tropical cyclones passing through an estuary’s watershed may
mobilize more nutrients and/or organic matter than those passing
over or skirting an estuary, thereby leading to more severe effects
on estuarine water quality (Mallin et al., 2002; Mallin and Corbett,
2006). The effects of floods and tropical cyclones may also depend
on post-event environmental conditions. For instance, Hickel et al.
(1993) observed large phytoplankton blooms in the German Bight
following floods in 1981, but not following floods in 1987–1988.
They attributed this differential response to differences in wind
Fig. 2. Abundance of seagrass (% cover) in Hervey Bay, Australia, prior to (a),
conditions following the floods. Calm winds followed the 1981
10 months after (b), and 22 months after massive flooding and passage of a
tropical cyclone (c). Stippling represents seagrass cover generalized from sampling floods, which interacted with freshwater input to allow for devel-
sites. These events led to severe light limitation and significant sediment opment of stratification and favorable light conditions for phyto-
resuspension that prolonged recovery of seagrass beds. Reprinted from: Preen, plankton. In contrast, strong winds followed the 1987–1988
A.R., Lee Long, W.J., Coles, R.G., 1995. Flood and cyclone related loss, and partial
floods, leading to significant vertical mixing and poor light condi-
recovery, of more than 1000 km2 of seagrass in Hervey Bay, Queensland, Australia.
Aquatic Botany 52, 3–17, with permission from Elsevier.
tions. Mallin et al. (2002) suggested that tropical cyclones which
strike temperate estuaries in late fall may have a less severe effect
on water quality than do those that occur during warmer summer
1993; Correll et al., 1999; Eyre and Ferguson, 2006; Cook et al., months. Cooler temperatures found in late fall should not only pro-
2010; Voynova and Sharp, 2012) can also lead to significant nutri- mote higher oxygen solubility, but also lead to reduced bacterial
ent loading in estuaries, where phytoplankton growth is often growth and degradation of freshwater-derived organic matter
nutrient limited (Cloern, 2001). Despite this, the phytoplankton re- (Mallin et al., 2002). Furthermore, light levels are lower in late fall,
sponse to these nutrient-loading events is not straightforward. For which may prevent large-scale phytoplankton blooms from
instance, high turbidity in flood waters and rapid flushing, which forming. Unfortunately, little information is available on the influ-
tend to be most pronounced in the days and weeks following these ence of tropical cyclone or flood characteristics on estuarine water
150 9
DIN Anomaly (µM) Flow anomaly (m³ s-¹)
Salinity Anomaly
100 6
3
50
0
0
-3
-50 -6
-100 -9
25 50
Chl Anomaly (µg L-1)

15 25
5
0
-5
-25
-15
-25 -50
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
0.8
0.6
Kd Anomaly (m-1)
0.4
0.2
0.0
-0.2
-0.4
-0.6
-0.8
2000
2001
2002
2003
2004
2005
2006
2007
2008
2009
Fig. 3. Mean monthly anomalies of river flow, salinity, dissolved inorganic nitrogen, chlorophyll a, and light attenuation (Kd) in North Carolina’s Neuse River Estuary.
‘‘Anomaly’’ refers to the deviation from a long-term (2000–2009) monthly average. Positive Kd indicates higher than average light attenuation. Included in this time series are
two drought periods (2001–2002, 2007–2008) and two periods of above average precipitation and river flow (2003, late 2006–early 2007). For additional details on study
design, see: Wetz, M.S., Hutchinson, E., Lunetta, R., Paerl, H.W., Taylor, J.C., 2011. Severe droughts reduce planktonic production in estuaries with cascading effects on higher
trophic levels. Limnol. Oceanogr. 56, 627–638.
quality. Thus many of the aforementioned relationships need fur- anthropogenic nutrient loading may sustain ecosystem productiv-
ther verification through sustained observations that allow for ity during extreme low freshwater inflow events. However, it re-
comparison of the effects of different events on the water quality mains to be determined whether the ecosystem behaves the
of a given system. same in these conditions as opposed to under more normal fresh-
In addition to the nutrient and organic matter loading that may water inflow regimes, especially considering that point-source
accompany tropical cyclones and floods, there is growing concern anthropogenic nutrients are qualitatively/functionally different
about other contaminants such as microbial pathogens. A number than watershed-derived nutrients and may lead to phytoplankton
of studies have noted significant loading and/or enhancement of blooms that are harmful to the ecosystem (e.g., Anderson et al.,
in situ growth of fecal coliforms (Weiskel et al., 1996; Lipp et al., 2002; Nixon, 2003).
2001; Chigbu et al., 2004; Coulliette and Noble, 2008), enterovirus- There are examples of estuarine systems that do not follow the
es (Lipp et al., 2001), and Vibrio spp. (Wetz et al., 2008; Lara et al., general trend of reduced phytoplankton biomass or productivity
2009) following tropical cyclone passage or floods. As will be dis- during low freshwater inflow conditions. One complicating factor
cussed later, loading of these pathogens via stormwater appears is that freshwater inflow often has a significant modulating effect
to be exacerbated in highly urbanized settings. on residence time as well. In the eutrophic Hudson River Estuary
for example, persistent high nutrient loads only lead to significant
2.1.2. Drought phytoplankton productivity during extended periods of low flow.
Limited studies on extreme low freshwater inflow events sug- This reduces advection of phytoplankton via increased residence
gest that these events may affect estuarine water quality in a man- time and also increases stratification that improves the light envi-
ner dissimilar to high freshwater inflow events, namely by ronment for phytoplankton (Howarth et al., 2000). Temporarily
improving it. Less freshwater inflow should theoretically equate open/closed coastal (estuarine) lakes of South Africa, Australia
to reduced allochthonous organic matter and nutrient inputs, and and New Zealand are affected not only by freshwater inflow but
also reduced phytoplankton bloom activity. also by flushing associated with intermittent opening of their
Several studies have in fact shown a general decrease in nutri- mouth, allowing for exchange with coastal seawater. As such, com-
ent loading, phytoplankton productivity and/or biomass during ex- plex water quality and phytoplankton responses are often ob-
tended periods of below average freshwater inflow (e.g., Cloern served that depend on both freshwater inflow and exchange with
et al., 1983; Nixon, 2003; Boynton et al., 2008; Lin et al., 2008; coastal waters, with closing of the mouths often leading to in-
Abreu et al., 2010; Phlips et al., 2010; Wetz et al., 2011; Fig. 3). creased residence time, accumulation of nutrients and phytoplank-
In a situation perhaps analogous to a prolonged drought, freshwa- ton biomass (e.g., Taljaard et al., 2009; Perissinotto et al., 2010;
ter discharge to the Nile Delta decreased by >90% and seasonal Schallenberg et al., 2010).
phytoplankton blooms ceased to develop after construction of Water quality data from Wetz et al. (2011) highlights the effects
the Aswan Dam on the Nile River in the 1960s (Nixon, 2003). In re- of variable freshwater inflow on water quality in a spatially-
cent years, the productivity of the Nile Delta has recovered some- explicit manner, indicating that while the scenario of drought-
what, not as a result of restored freshwater inflow but instead from induced reductions in nutrient inputs and phytoplankton activity
significant increases in anthropogenic nutrient loadings (Nixon, generally holds true, the relationship is somewhat more compli-
2003). This is an interesting scenario that suggests enhanced cated. For instance, during two droughts that affected North
Carolina’s Neuse River Estuary during the 2000s, phytoplankton accompanying ECE (see also Baldwin et al., 2005). A biological
productivity and biomass were below average and bottom water example pointing to the importance of drought–flood sequences
dissolved oxygen was above average over a substantial portion of comes from the lower Chesapeake Bay and tributaries. In 2007, a
the estuary during drought, but phytoplankton productivity was massive bloom of the icthyotoxic dinoflagellate, Cochlodinium poly-
actually enhanced and bottom water dissolved oxygen was below krikoides, developed coincident with a period of heavy rains that
average in the upper estuary due to upstream migration of the followed a drought and low nutrient inputs (Mulholland et al.,
estuarine chlorophyll maxima (Wetz et al., 2011). Thus from an 2009). The authors suggest this sequence allowed C. polykrikoides
estuarine habitat management perspective, water quality may im- to gain relative importance over other phytoplankton because of
prove in some areas of an estuary while deteriorating in others as a its ability to utilize organic nutrients during the drought; hence,
result of drought. when even more favorable conditions developed (i.e., high inor-
Several authors have also noted above average estuarine dis- ganic and organic nutrient loads accompanying the heavy rains),
solved oxygen levels during drought (e.g., Livingston et al., 1997; it was primed for bloom formation. These limited examples high-
Attrill and Power, 2000a; Boynton et al., 2008; Lin et al., 2008; light the importance of not only quantifying the effects of specific
Wetz et al., 2011), attributing this to reduced stratification and re- events, but also the necessity for examining differences in estua-
duced deposition of phytodetritus. Another possibility may be in- rine water quality response that may be attributed to the sequence
creased benthic primary production. Increased light penetration of events. This will require sustained observations and highlights
is often an artifact of reduced freshwater inflow and/or reduced the importance of coastal time-series studies that focus on key
water column phytoplankton biomass (Livingston et al., 1997; organisms and ecological processes.
Wetz et al., 2011; Fig. 3) and may favor the growth of, and oxygen
production by, benthic microalgae or other benthic primary pro- 2.1.4. Heat waves
ducers (Rask et al., 1999; Fear et al., 2004; Stutes et al., 2006; A number of important water quality-related processes are pos-
Krause-Jensen et al., 2007; Murrell et al., 2009). There is almost itively correlated with temperature in estuaries, including (but not
no information available on the response of benthic primary pro- limited to) bacterial respiration and oxygen demand in subpycno-
ducers to sharp reductions in freshwater inflow, though the afore- cline waters (Stanley and Nixon, 1992; Cowan and Boynton,
mentioned studies point to a necessity for more research focusing 1996; Borsuk et al., 2001) and microbial pathogen growth (Motes
on coupled benthic and pelagic primary producer responses to et al., 1998; Pfeffer et al., 2003; Hsieh et al., 2008). Yet few studies
changes in freshwater inflow. have specifically focused on the effects of heat waves. The few stud-
Despite generally positive effects on estuarine water quality, ies that are available all suggest a generally negative effect of heat
low freshwater inflow events may still have deleterious effects waves on estuarine water quality. For instance, several potentially
on living resources. Most apparent are effects of these events on toxic cyanobacteria species thrive at high temperatures (reviewed
the physical–chemical conditions in estuaries (e.g., salinity, marsh by Paerl et al. (2011)). One example comes from northern Europe,
chemistry, etc.) and subsequent implications for habitat suitability. where during a recent heat wave massive blooms of Microcystis, a
For example, several recent studies have noted dieback of salt toxin producing cyanobacteria, were observed in estuarine waters
marsh grasses during droughts (Mckee et al., 2004; Alber et al., (Johnk et al., 2008). Concerns are also mounting over the synergistic
2008). Although the cause of these diebacks is unknown, at least effects of high temperatures and increasing carbon dioxide levels in
one study suggested that there are direct and negative effects of the atmosphere, which may further act to intensify cyanobacterial
drought on marsh grass physiology (Brown et al., 2006). Similarly, blooms (Paerl et al., 2011). Stimulatory effects of high temperatures
a recent study documented major declines in seagrass biomass have also been noted on pathogenic microbies in coastal waters. For
during drought (Cardoso et al., 2008). example, in Israeli coastal waters, a major outbreak of V. vulnificus
Drought also appears to create conditions favorable for certain occurred coincident with a record heat wave (Paz et al., 2007).
bivalve pathogens, namely Haplosporidium and Perkinsus, as has These outbreaks of harmful microbes point to the risks associated
been noted by the inter- and intra-estuary range expansion of with heat waves and emphasize the need for further study of
these organisms during droughts (Burreson and Calvo, 1996; time-series data that emphasizes species-specific responses to elu-
Burreson and Ford, 2004; Bushek et al., 2012). Drought also favors cidate the ecological effects of heat waves. These examples also
many predators of bivalves, hence during drought severe mortality highlight the importance of developing emerging technologies for
of commercially and ecologically-important shellfish is often rapid quantification of harmful species and/or their toxins.
observed due to both predation and disease (e.g., Buzan et al.,
2009; Petes et al., 2012). In regards to human pathogens, recent 2.1.5. Summary
studies conducted in several North Carolina estuaries suggests that
the abundance of the pathogen Vibrio vulnificus may be greatly re- Tropical cyclones and floods often have a net negative effect on
duced during drought relative to above average freshwater inflow estuarine water quality by causing significant organic matter,
conditions (Wetz and Noble, submitted for publication; Froelich nutrient and pathogen loading, as well as deoxygenation of
et al., 2012). estuarine waters. One positive aspect of tropical cyclone pas-
sage is the wind-driven disruption of subpycnocline hypoxia
2.1.3. Interactions between droughts and tropical cyclones/floods that is facilitated by stratification (Rabalais et al., 2009), though
Few studies have examined the interactive effects of ECE, this immediate benefit may be negated by the aforementioned
though there are intriguing examples which suggest that the se- longer-term negative effects of tropical cyclones.
quence of drought–cyclone/flood events may significantly affect Severity of water quality changes caused by tropical cyclone
estuarine water quality. For example, Kaushal et al. (2008) ob- passage may depend on location of landfall and cyclone
served high nitrogen export during wet conditions that followed trajectory.
a drought in a Chesapeake Bay watershed, implying that nitrogen Effects of tropical cyclones and floods may depend on their tim-
is stored in soils and other reservoirs within the watershed during ing as well as post-event environmental conditions.
drought. Likewise, Sigleo and Frick (2007) observed very high ni- Droughts influence water quality by altering freshwater inflow,
trate export from a coastal Oregon watershed during the first watershed nutrient/organic matter loading, residence time and
storm that followed a prolonged drought. Thus, the sequence of ultimately phytoplankton activity. Positive and negative effects
events may affect the relative magnitude of nutrient loading of drought on water quality have been documented.
Droughts can reduce habitat suitability for important estuarine 2.2.1. Summary
organisms by induction of physiological stress or promotion of
pathogen outbreaks. Water quality changes induced by tropical cyclones and floods
The effects of drought and tropical cyclones/floods are modu- are of much shorter duration (days to few months) than those
lated by the sequence in which these events occur. from drought (months to years).
High temperatures, such as during heat waves, stimulate a Differences may exist in the water quality response within mac-
number of important ecological processes, many of which have rotidal versus microtidal estuaries to cyclone or flood events.
negative consequences for estuarine water quality.
2.3. Is there a relationship between land-use coverage in estuarine
watersheds and ECE-induced water quality changes?
2.2. How long do the effects of ECE persist, and how does this depend
on the tidal regime of affected estuaries? Conversion of natural forested lands to urban area or agricul-
tural land can alter water quality of adjacent rivers and estuaries
Tropical cyclones and floods tend to elicit fairly short-lived (Hopkinson and Vallino, 1995; Carpenter et al., 1998). For example,
water quality changes in estuaries (Valiela et al., 1998; Eyre and Peierls et al. (1991) demonstrated that nitrate export in rivers in-
Ferguson, 2006; Hagy et al., 2006; Tomasko et al., 2006; Dix creased precipitously as human population in watersheds in-
et al., 2008). For instance, Tomasko et al. (2006) and Dix et al. creased. More recently, efforts have been put forth to better
(2008) examined the effects of several major tropical cyclones that understand the effects of different types of land use on material ex-
passed through Florida in 2004. In central Florida, Tomasko et al. port. A number of studies have now observed relatively higher or-
(2006) found that cyclone-derived changes in water quality lasted ganic carbon and/or organic nitrogen loads associated with
<2 weeks. As a result of the same cyclones passing over a north agricultural or urbanized watersheds compared to forested water-
Florida estuary, Dix et al. (2008) found that cyclone-induced organ- sheds (Howarth et al., 1991; Jordan et al., 2003; Rothenberger
ic matter and nutrient loading lasted for <1 month. Following et al., 2009; but see Mallin et al., 2009). Similarly, inorganic nutri-
Hurricane Ivan’s passage over Florida’s Pensacola Bay, Hagy et al. ent (N and P) export tends to be elevated in agricultural or urban-
(2006) observed development of a modest phytoplankton bloom, ized watersheds compared to forested watersheds (Vernberg et al.,
which again lasted <1 month. Likewise, cyclone-induced blooms 1992; Bowen and Valiela, 2001; Jordan et al., 2003; Handler et al.,
noted in Wetz and Paerl (2008) also tended to last <1 month. How- 2006; Kaushal et al., 2008; Mallin et al., 2009; Rothenberger et al.,
ever, back-to-back cyclones may elicit a much more severe water 2009). In addition to affecting biogeochemical dynamics, land use
quality response. For instance, three cyclones struck eastern North coverage and change can significantly affect microbial pathogen
Carolina in late summer–fall 1999, leading to severe flooding that loading. There is ample evidence pointing to agricultural or urban-
lasted several months and that stimulated large phytoplankton ized lands as being a relatively greater source of fecal coliform
blooms in a coastal embayment, Pamlico Sound, that lasted loading to adjacent waterbodies than forested lands (Vernberg
6 months (Paerl et al., 2001; Peierls et al., 2003). The longest lived et al., 1992; Mallin et al., 2000, 2001, 2009; Holland et al., 2004;
effects of tropical cyclones and floods may be on seagrass commu- Handler et al., 2006; Campos and Cachola, 2007; DiDonato et al.,
nities. In those instances where severe loss of seagrass beds was 2009). Impervious surface associated with urbanization is a partic-
noted to occur following tropical cyclone passage or flooding, it ularly important driver of water quality. A study in eastern North
took several years for the seagrass to recover (Preen et al., 1995; Carolina showed that streams and estuaries adjacent to highly
Campbell and Mckenzie, 2004). urbanized areas experienced proportionally greater stormwater
The overall susceptibility of an estuarine ecosystem to tropical runoff, nutrient and fecal coliform loads and biological oxygen de-
cyclone and flood effects may depend on an estuary’s tidal regime. mand than those with forested watersheds (e.g., Mallin et al.,
In some cases, affected estuarine waters can be rapidly diluted via 2009). However, in contrast to those findings from microtidal estu-
exchange with relatively oligotrophic coastal waters following aries in North Carolina, van Dolah et al. (2008) did not observe
tropical cyclone passage (Tomasko et al., 2006; Edmiston et al., strong relationships between watershed urbanization and water
2008). Similarly, Caffrey et al. (2007) observed stimulation of phy- quality in South Carolina tidal creeks, perhaps suggesting that tidal
toplankton production but not biomass in response to freshwater flushing may limit prolonged deleterious effects of stormwater
nutrient pulses in Elkhorn Slough estuary, California. Those authors pulses.
argued that the lack of phytoplankton biomass accumulation was Through the synergism between land use coverage, stormwater
due to the rapid tidal flushing of this estuary, which is consistent pulses, and tidal flushing, future increases in ECE may cause as yet
with the analysis of Monbet (1992). Cross-ecosystem comparative unpredictable effects on estuarine ecosystems. The contrasting re-
studies are merited to better understand the relationship between sults of van Dolah et al. (2008) and Mallin et al. (2009) for example,
tidal flushing and cyclone or flood effects. This mechanistic under- suggest that more studies are needed on the relationship between
standing will be necessary to assess the vulnerability to these ef- land use coverage, estuarine tidal flushing and water quality, per-
fects for the broad range of estuaries as classified according to haps through comparative studies of estuaries that vary in terms of
degree of tidal flushing. their degree of tidal flushing. To date, there have been few studies
When one compares the duration (3–6 months) of water qual- that compare water quality responses to ECE across multiple estu-
ity perturbations caused by even the most severe back-to-back aries that vary in land use coverage or tidal flushing.
tropical cyclones with those of recent droughts (>6 months), it ap-
pears that drought elicits a much more prolonged ecosystem re- 2.3.1. Summary
sponse. Wetz et al. (2011) found that the ecological effects of a
drought that began in mid-2007 and officially ended mid-2008 Estuaries with agricultural or urbanized watersheds experience
actually lasted well into 2009. Paleoclimate records suggest that relatively more severe water quality degradation from tropical
naturally occurring droughts lasting 10 years or more have oc- cyclone passage or flooding than estuaries with forested
curred quite regularly in the eastern United States during the past watersheds.
1600 years (Stahle et al., 1988; Cronin et al., 2000), accompanied The degree of tidal flushing appears to affect the magnitude of
by water quality changes in affected estuaries (Cronin and Vann, water quality changes induced by tropical cyclone passage or
2003). flood events. Limited evidence suggests that microtidal estuar-
ies with urbanized watersheds may experience relatively more watersheds (e.g., Najjar et al., 2010). The ability to accomplish this
severe water quality degradation from tropical cyclone passage important task necessitates improvement of regional climate pro-
or flooding than macrotidal estuaries with urbanized jections (Najjar et al., 2010), as global climate models are of limited
watersheds. use at regional or single-estuary scale due to uncertainties in-
volved in downscaling precipitation patterns (Schiermeier, 2010;
3. An extreme future for estuaries? Maraun et al., 2010) and in tropical cyclone projections (Bender
et al., 2010).
Climate projections suggest the possibility of more frequent As highlighted in our review, there are fundamental gaps in our
and/or intense high precipitation events, drought and heat waves scientific understanding of mechanistic linkages between climate
in the near future as a result of anthropogenic greenhouse gas variability (incl. ECE), other environmental changes (i.e., land
emissions (Meehl et al., 2007). For example, model projections use), estuarine water quality and ecological dynamics that hinder
from the most recent Intergovernmental Panel on Climate Change efforts to project future changes to estuarine ecosystem dynamics.
(IPCC) report suggest that air temperatures in coastal regions One reason may be a lack of dedicated funding due to the potential
worldwide are expected to rise from 2 to 5 °C during the 21st cen- damaging effects on research infrastructure and significant risks
tury (Christensen et al., 2007). As such, the models project that involved (in the case of tropical cyclones and floods) (e.g., Lindem-
prolonged heat waves will become more common in the future ayer et al., 2010). Lack of coastal time-series studies encompassing
(Meehl et al., 2007). Concurrently, drought may become more fre- a sufficient suite of systems, environmental parameters, and sam-
quent due to higher evapotranspiration rates and shifting precipi- pling locations within particular systems and their watersheds cre-
tation patterns. Regions of particular concern for intensification of ates an additional challenge to quantifying environmental change
drought include both northern and southern Africa, southern in the coastal zone, and more specifically for understanding effects
Europe and the greater Mediterranean region, west-central Asia of ECE. For example, the most extensive US water quality monitor-
(Middle East), the western Gulf of Mexico, greater Caribbean re- ing program, the National Estuarine Research Reserve (NERR) pro-
gion, and southern Australia (Christensen et al., 2007). Climate gram, includes study sites from nearly every coastal state in the US.
models also project a trend towards more intense precipitation At present, most NERR sites deploy instrumentation to continu-
events, at least a seasonal basis and possibly throughout the year, ously monitor basic water quality parameters (i.e., temperature,
in regions such as west central and east central Africa, northern salinity, pH, dissolved oxygen), but could address a broader suite
Europe, Asia (east, northeast, southern), the US Atlantic coast, of ecological questions if given the ability to incorporate modern,
and possibly eastern South America (Christensen et al., 2007). but practical, technologies for continuous monitoring of other
Finally, there are indications that tropical cyclones may become parameters (i.e., chlorophyll a and/or biomarker pigments,
more intense but less frequent over the coming century (e.g., Richardson et al., 2010; nutrients and organic matter, Conmy
Elsner et al., 2008; Knutson et al., 2010). Consequently, it is con- et al., 2004; Jannasch et al., 2008; Plant et al., 2009). Additionally,
ceivable that ECE will be an ever more important driver of estua- many NERR locations are constrained by logistics and funding to
rine ecosystem function and water quality in the near future. It is only deploying monitoring equipment and/or collecting discrete
important to note that evidence is emerging that many of the pro- samples at a few fixed sites. But if these efforts could be expanded
jected changes to heat wave frequency, drought and flood cycles to include a further subset of sampling sites along the estuarine
may already be underway (e.g., Min et al., 2011; Pall et al., 2011; salinity gradient, this could prove to be a powerful tool for charac-
Trenberth and Fasullo, 2012; Trenberth, 2012), adding a degree terizing the whole estuary response to climatic and/or anthropo-
of urgency to efforts to understand their effects on ecosystems, genic changes. Similar constraints have been documented in
including estuaries. European estuaries as well (de Jonge et al., 2006). At a larger scale,
Anthropogenic climate change will be superimposed on sub- creation of integrated regional and continental scale sampling net-
stantial increases in human populations living in coastal water- works that include not only estuaries but their watersheds would
sheds. According to the 2010 revision of the United Nations represent a major step forward towards recognizing and under-
population projections, the world population will surpass 9 billion standing the critical role that watersheds will play in modulating
people by the year 2050 and 10 billion people by 2100 (United the future direction of environmental changes in estuaries (e.g.,
Nations, 2011). At present it is estimated that 40% of the world’s de Jonge et al., 2006; Hopkinson et al., 2008).
population lives within 100 km of the coast (CIESIN, 2012). Assum- Despite challenges associated with projecting the response of
ing no changes in these percentages and population growth esti- estuaries to ECE, here we offer two potential scenarios based upon
mates, 4 billion people could be living along the world’s coasts general historic or contemporaneous patterns observed in estuar-
by 2100 versus 2.8 billion today. Anthropogenic climate change ies, as previously highlighted in our review. The first emphasizes
and projected increases in human populations in the coastal zone the potential effects of more intense tropical cyclone strikes or
will have far reaching implications for water cycles and estuarine flood events, while the second emphasizes the potential effects of
ecosystem dynamics, as climate drivers such as ECE interact with prolonged low freshwater inflow conditions.
anthropogenic change (land use, nutrient loading) to strongly af-
fect estuarine water quality and overall estuarine ecosystem health 3.1. Effects of more intense tropical cyclones and floods
(Scavia et al., 2002; Flemer and Champ, 2006; Paerl et al., 2006).
These changes may be tempered or amplified by natural climate Model projections from several recent studies converge on a
cycles, such as those associated with ENSO, the North Atlantic solution of more intense cyclones and high precipitation events
Oscillation, Pacific Decadal Oscillation and other modes of climate as a result of global climate change (Meehl et al., 2007; Elsner
variability (e.g., Cloern et al., 2007; Kimmel et al., 2009; Barbosa et al., 2008; Bender et al., 2010). Thus it is worthwhile to offer a
et al., 2010; Pollack et al., 2011; Bushek et al., 2012), pointing to broad scenario for the effects of stronger cyclones or precipitation
a need for considering these factors in totality, as opposed to in iso- (flood) events. It is conceivable that infrastructural damage (i.e., to
lation (Fig. 1; Table 1). An important long-term goal for estuarine municipal wastewater facilities, animal waste lagoons) will be-
resource managers is to project estuarine ecosystem responses to come more common as a result of winds and flooding at inland
various environmental change scenarios, including more frequent locations and as a result of winds, flooding and enhanced storm
or intense ECE, ever increasing human freshwater demands, land surge (resulting from sea-level rise) near the coast. This problem
use changes (urbanization) and nutrient enrichment of coastal is likely to be most pronounced in developing nations, which are
Table 1
Summary of the short- and long-term effects of extreme climatic events on select water quality indicators. ; indicates negative effect, M indicates neutral effect, " indicates
positive effect, sp. indicates potential for species-specific responses, and ? indicates not enough data available to pass judgment.
Water quality indicator Short-term (days– Long-term (months–

weeks) effects years) effects
Phytoplankton and harmful algal bloom growth (via interaction between nutrient loading, light attenuation, Cyclone and flood: ; "M;
stratification and residence time)
Drought: ;
Heat wave: "sp. "?sp.
Bottom water oxygenation (via interaction between organic matter loading, stratification, temperature and Cyclone and flood: "M; M
residence time)
Drought: "M
Heat wave: ;? ;?
Microbial pathogen growth (via interactions between pathogen loading, salinity and temperature) Cyclone and flood: " ?
Drought: ";sp.
Heat wave: "? "?
Seagrass or marsh grass health (via interactions between physical damage, physiological stress and light Cyclone and flood: ;M ;M
attenuation)
Drought: ;
Heat wave: ? ?
expected to see a major increase in wastewater facilities and asso- conditions, etc.; Duarte, 2002), may have severe negative effects on
ciated nutrient loadings over the coming decades due to popula- seagrasses and associated biological communities in affected estu-
tion growth (van Drecht et al., 2009), but which may lack arine systems (Preen et al., 1995). In conjunction with increased
resources to build weather-resistant facilities. It is also conceivable hypoxia potential, loss of critical seagrass habitat would represent
that on land, soil mobilization and flushing may be enhanced, an additional stressor upon coastal fish communities (Waycott
while scouring of sediments may be enhanced in riverine or estu- et al., 2009). Coincident with any negative effects on coastal fisher-
arine waterbodies (DeLaune and White, 2012; Yoon and Raymond, ies that may develop, side effects such as loss of tourism or recre-
2012). The net effect of infrastructural damages as well as in- ational fishing activity in response to the harmful water quality
creased soil and sediment scouring will be enhanced point- and changes induced by stronger tropical cyclones or flood events
non-point source nutrient and organic matter loadings to estuaries. should be anticipated. The potential impact on a broader suite of
Possible regulating factors include the frequency at which these ecosystem services must also be considered, such as reduction in
extreme precipitation events occur and/or prior climatic condi- coastal protection, erosion control, water purification, recreational
tions, as well as the rate and direction of land use changes in af- opportunities, carbon sequestration, and water purification (Barbi-
fected coastal watersheds. Stronger cyclones or flood events will er et al., 2011). These benefits can be significant, as pollution and
likely also lead to large-scale, prolonged stratification in estuaries poor water quality can reduce the value of trips to beaches and
as a result of freshwater input. In the short-term (days–weeks), for recreational fishing (Freeman, 1995; Kaoru, 1995; Massey
flushing and low light levels may prevent phytoplankton growth, et al., 2006), and can go as far as impacting residential land prices
though allochthonous organic matter loading will likely be signif- (Leggett and Bockstael, 2000).
icant. Strong stratification and elevated allochthonous organic
matter inputs, coupled with projected global temperature in- 3.2. Effects of intensified and/or more frequent low freshwater inflow
creases by the end of the 21st century, will create conditions favor- events
able for bottom water hypoxia formation that is rapid in
development, broadly distributed and persistent in time. Sediment Drought coupled with burgeoning human population growth in
resuspension and runoff-driven loading of pathogenic microbes, coastal watersheds puts severe strain on freshwater supplies and
coupled with warmer temperatures, create conditions favoring greatly reduces freshwater inflows to estuaries, especially when
widespread outbreaks of these organisms (Lipp et al., 2001; Coull- coincident with seasonal peaks in human freshwater demand
iette and Noble, 2008; Fries et al., 2008; Wetz et al., 2008). (e.g., Livingston et al., 1997; Meyer et al., 1999). Extreme low fresh-
In the longer-term (weeks–months), enhanced nutrient inputs water inflow events are becoming a global concern, with human
and relaxation of severe flushing conditions may act to stimulate activity (water diversion and usage) and climate change (drought)
widespread phytoplankton blooms, possibly including harmful al- interacting to modify the global water cycle and river flows, there-
gal bloom species. Upon reaching senescence, these blooms may by affecting delivery of freshwater to coastal regions (Meyer et al.,
further stimulate biological oxygen demand and hypoxia forma- 1999; Vorosmarty et al., 2000; Milliman et al., 2008; Palmer et al.,
tion or, in the case of harmful algal blooms, may release deleterious 2008). Future projections of more intense drought due to climate
compounds into the water column. From an ecosystem goods and change coupled with increasing human freshwater demand in
services standpoint, a reasonable focus is on the habitat and fisher- many world regions magnify these concerns (Gibson et al., 2005;
ies implications of more severe tropical cyclones and floods. Hyp- Flemer and Champ, 2006; Meehl et al., 2007; McDonald et al.,
oxic conditions alone can severely reduce habitat for a number of 2011).
commercially-important fish and shellfish species and lead to sig- Freshwater contains nutrients and organic matter that, upon
nificant localized, short-term mortality (e.g., Paerl et al., 2001). It is delivery to the coastal zone, fuels the rich productivity of coastal
quite possible that high, sustained loadings of sediment, allochth- ecosystems and shapes critical fish habitat through effects on
onous (riverine) and autochthonous (phytoplankton) organic mat- salinity gradients and stratification (e.g., Alber, 2002; Kimmerer,
ter will lead to a long-term (months) decline in light penetration. 2002; Nixon, 2003). Thus, extreme low freshwater inflow events
This, in conjunction with other environmental stressors (i.e., sea le- have the potential to significantly alter estuarine ecosystem struc-
vel rise and associated erosional forces, unfavorable water quality ture, function, and overall water quality (Livingston et al., 1997;
Attrill and Power, 2000b; Pollack et al., 2011; Wetz et al., 2011). In fect functioning of a particular estuarine system, and societal ac-
Texas, a natural climatic gradient exists where freshwater inflow tions that may arise in response to managed and unmanaged
decreases >50-fold moving south from the Louisiana to Mexico changes to estuarine ecosystems and their services (see e.g., Atkins
border (Montagna et al., 2007). Nitrogen loads decrease and salin- et al., 2011; Fig. 1). Implicit in this is the necessity for understand-
ity increases concurrent with the decreasing freshwater inflow, ing mechanistic linkages between ECE and estuarine water quality
and likewise shellfish harvests decrease by 20-fold, though the and ecosystem dynamics.
mechanistic linkages between freshwater inflow and changes in
shellfish harvest are not well understood. In North Carolina’s Neuse Acknowledgements
River Estuary, nitrogen loads, phytoplankton productivity and zoo-
plankton biomass were all sharply lower during drought condi- We thank Drs. Alan Lewitus and Jennifer Beseres Pollack for
tions as opposed to non-drought conditions, adult fish mortality constructive comments on an earlier version of this manuscript.
was higher by >2-order of magnitude, and commercial fish land- Financial support was provided by grants from the National
ings were lower during drought (Wetz et al., 2011; Wetz, unpubl. Science Foundation (DEB 1104598, OCE 0726989) to MSW and
data). Similarly, during a prolonged drought in Apalachicola Bay, from the National Oceanic and Atmospheric Administration under
Florida, Livingston et al. (1997) observed significant reductions in the Comparative Assessment of Marine Ecosystem (CAMEO)
the biomass of several higher trophic level functional guilds and Program to DWY (NA09NMF4720179).
speculated that this was due, in part, to reduced primary and sec-
ondary productivity and consequently food for the higher trophic
References
levels. Livingston et al. (2000) noted a strong negative effect of
drought on oysters, presumably due to higher salinities, increased Abreu, P.C., Bergesch, M., Proenca, L.A., Garcia, C.A.E., Odebrecht, C., 2010. Short- and
disease and predation. After construction of the Aswan Dam on long-term chlorophyll a variability in the shallow microtidal Patos Lagoon
Egypt’s Nile River, freshwater discharge to the Nile delta decreased estuary, southern Brazil. Estuar. Coasts 33, 554–569.
Alber, M., 2002. A conceptual model of estuarine freshwater inflow management.
by >90%, seasonal phytoplankton blooms no longer developed and Estuaries 25, 1246–1261.
fish and shrimp landings decreased by 50–100% relative to pre- Alber, M., Swenson, E.M., Adamowicz, S.C., Mendelssohn, I.A., 2008. Salt marsh
dam conditions (Nixon, 2003). In the US southwest, reductions of dieback: an overview of recent events in the U.S. Estuar. Coast. Shelf Sci. 80,
1–11.
freshwater inflow to the Colorado River Delta have been linked Anderson, D.M., Glibert, P.M., Burkholder, J.M., 2002. Harmful algal blooms and
to significant (94%) reductions in bivalve densities compared to eutrophication: nutrient sources, composition and consequences. Estuaries 25,
historical periods of natural river flow (Kowalewski et al., 2000). 704–726.
Anton, A., Cebrian, J., Duarte, C.M., Heck, K.L., Goff, J., 2009. Low impact of Hurricane
In Texas, a 10-year drought that began in the late 1940s also led
Katrina on seagrass community structure and functioning in the northern Gulf
to significant declines in estuarine oyster, shrimp and blue crab of Mexico. Bull. Mar. Sci. 85, 45–59.
harvests (Copeland, 1966). Atkins, J.P., Burdon, D., Elliott, M., Gregory, A.J., 2011. Management of the marine
These findings highlight both the habitat and trophic impor- environment: integrating ecosystem services and societal benefits with the
DPSIR framework in a systems approach. Mar. Pollut. Bull. 62, 215–226.
tance of adequate freshwater inflow conditions. Ultimately, effects Attrill, M.J., Power, M., 2000a. Modelling the effect of drought on estuarine water
of reduced freshwater inflow on ecosystem goods and services may quality. Water Res. 34, 1584–1594.
range from the obvious (i.e., altered nutrient cycling; lost recrea- Attrill, M.J., Power, M., 2000b. Effects on invertebrate populations of drought-
induced changes in estuarine water quality. Mar. Ecol. Prog. Ser. 203, 133–143.
tional and commercial fishing and shellfishing opportunities) to Baldwin, D.S., Rees, G.N., Mitchell, A.M., Watson, G., 2005. Spatial and temporal
more subtle (i.e., changes in coastal erosion and protection, Koch variability of nitrogen dynamics in an upland stream before and after a drought.
et al., 2009). Nonetheless, there is a clear inherent value in ade- Mar. Freshwater Res. 56, 457–464.
Bales, J.D., 2003. Effects of Hurricane Floyd inland flooding, September–October
quate freshwater inflow to estuaries, yet this continues to be over- 1999, on tributaries to Pamlico Sound, North Carolina. Estuaries 26, 1319–1328.
looked in the growing policy debate over human versus ecosystem Barbier, E.B., Hacker, S.D., Kennedy, C., Koch, E.W., Stier, A.C., Silliman, B.R., 2011.
necessity for this vital resource (see e.g., Gillson, 2011). The value of estuarine and coastal ecosystem services. Ecol. Monogr. 81, 169–
193.
Barbosa, A., Domingues, R.B., Galvão, H.M., 2010. Environmental forcing of
phytoplankton in a Mediterranean estuary: (Guadiana Estuary, southwestern
4. Conclusions Iberia): a decadal study of anthropogenic and climate influences. Estuar. Coasts
33, 324–341.
Bell, S.S., Fonseca, M.S., Kenworthy, W.J., 2008. Dynamics of a subtropical seagrass
ECE are not only major drivers of estuarine water quality and landscape: links between disturbance and mobile seed banks. Landsc. Ecol. 23,
ecological dynamics, but also affect a number of important ecosys- 67–74.
tem goods and services derived from estuaries, such as fisheries Bender, M.A., Knutson, T.R., Tuleya, R.E., Sirutis, J.J., Vecchi, G.A., Garner, S.T., Held,
I.M., 2010. Modeled impact of anthropogenic warming on the frequency of
production, recreational opportunities, erosion control, and carbon intense Atlantic hurricanes. Science 327, 454–458.
sequestration. Even considering uncertainties in projections of fu- Borsuk, M.E., Stow, C.A., Luettich, R.A., Paerl, H.W., Pinckney, J.L., 2001. Modelling
ture ECE, contemporaneously they represent a naturally occurring oxygen dynamics in an intermittently stratified estuary: estimation of process
rates using field data. Estuar. Coast. Shelf Sci. 52, 33–49.
aspect of the global climate system. Furthermore, the likelihood of Bowen, J.L., Valiela, I., 2001. The ecological effects of urbanization of coastal
reaching a global agreement in the near-term to curb CO2 emis- watersheds: historical increases in nitrogen loads and eutrophication of
sions and prevent projected changes in ECE frequency or intensity Waquoit Bay estuaries. Can. J. Fish. Aquat. Sci. 58, 1489–1500.
Boynton, W.R., Hagy, J.D., Cornwell, J.C., Kemp, W.M., Greene, S.M., Owens, M.S.,
remains uncertain at best, and evidence has arisen suggesting that Baker, J.E., Larsen, R.K., 2008. Nutrient budgets and management actions in the
these changes may already be occurring. Thus resource managers Patuxent River estuary, Maryland. Estuar. Coasts 31, 623–651.
may face a growing challenge of balancing the provisioning of Briceno, H.O., Boyer, J.N., 2010. Climatic controls on phytoplankton biomass in a
subtropical estuary, Florida Bay, USA. Estuar. Coasts 33, 541–553.
important estuarine ecosystem goods and services with changes Brown, C.E., Pezeshki, S.R., DeLaune, R.D., 2006. The effects of salinity and soil drying
in ecosystem structure and function as a result of ECE and other on nutrient uptake and growth of Spartina Alterniflora in a simulated tidal
co-occurring environmental changes. Proactive efforts for increas- system. Environ. Exp. Bot. 58, 140–148.
Burkholder, J., Eggleston, D., Glasgow, H., Brownie, C., Reed, R., Janowitz, G., Posey,
ing the resiliency of estuaries to harmful effects of ECE will need to
M., Melia, G., Kinder, C., Corbett, R., Toms, D., Alphin, T., Deamer, N., Springer, J.,
be conducted in the context of broader ecosystem-based manage- 2004. Comparative impacts of two major hurricane seasons on the Neuse River
ment efforts which integrate, among other factors, the various and western Pamlico Sound ecosystems. Proc. Natl. Acad. Sci. USA 101, 9291–
stressors facing particular systems (i.e., climate change, eutrophi- 9296.
Burkholder, J.M., Glibert, P.M., Skelton, H.M., 2008. Mixotrophy, a major mode
cation, freshwater withdrawals, sea level rise, etc.), man’s needs of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8,
from a goods and services standpoint that are derived from or af- 77–93.
Burreson, E.M., Calvo, L.M.R., 1996. Epizootiology of Perkinsus marinus disease of Duarte, C.M., 2002. The future of seagrass meadows. Environ. Conserv. 29, 192–
oysters in Chesapeake Bay, with emphasis on data since 1985. J. Shellfish Res. 206.
15, 17–34. Edmiston, H.L., Fahrny, S.A., Lamb, M.S., Levi, L.K., Wanat, J.M., Wren, K., Selly, N.C.,
Burreson, E.M., Ford, S.E., 2004. A review of recent information on the 2008. Tropical storm and hurricane impacts on a Gulf Coast estuary:
Haplosporidia, with special reference to Haplosporidium nelson (MSX disease). Apalachicola Bay, Florida. J. Coast. Res. 55, 38–49.
Aquat. Living Resour. 17, 499–517. Elsner, J.B., Kossin, J.P., Jagger, T.H., 2008. The increasing intensity of the strongest
Bushek, D., Ford, S.E., Burt, I., 2012. Long-term patterns of an estuarine pathogen tropical cyclones. Nature 455, 92–95.
along a salinity gradient. J. Mar. Res. 70, 225–251. Eyre, B.D., Ferguson, A.J.P., 2006. Impact of a flood event on benthic and pelagic
Buzan, D., Lee, W., Culbertson, J., Kuhn, N., Robinson, L., 2009. Positive relationship coupling in a sub-tropical east Australian Estuary (Brunswick). Estuar. Coast.
between freshwater inflow and oyster abundance in Galveston Bay, Texas. Shelf Sci. 66, 111–122.
Estuar. Coasts 32, 206–212. Fear, J., Gallo, T., Hall, N., Loftin, J., Paerl, H., 2004. Predicting benthic microalgal
Caffrey, J.M., Chapin, T.P., Jannasch, H.W., Haskins, J.C., 2007. High nutrient pulses, oxygen and nutrient flux responses to a nutrient reduction management
tidal mixing and biological response in a small California estuary: variability in strategy for the eutrophic Neuse River Estuary, North Carolina, USA. Estuar.
nutrient concentrations from decadal to hourly time scales. Estuar. Coast. Shelf Coast. Shelf Sci. 61, 491–506.
Sci. 71, 368–380. Flemer, D.A., Champ, M.A., 2006. What is the future fate of estuaries given nutrient
Campbell, S.J., McKenzie, L.J., 2004. Flood related loss and recovery of intertidal over-enrichment, freshwater diversion and low flows? Mar. Pollut. Bull. 52,
seagrass meadows in southern Queensland, Australia. Estuar. Coast. Shelf Sci. 247–258.
60, 477–490. Freeman, A.M., 1995. The benefits of water quality improvements for marine
Campos, C.J.A., Cachola, R.A., 2007. Faecal coliforms in bivalve harvesting areas of recreation: a review of the empirical evidence. Mar. Resour. Econ. 10, 385–
the Alvor lagoon (Southern Portugal): influence of seasonal variability and 406.
urban development. Environ. Monit. Assess. 133, 31–41. Fries, J.S., Characklis, G.W., Noble, R.T., 2008. Sediment–water exchange of Vibrio sp.
Cardoso, P.G., Rafaelli, D., Pardal, M.A., 2008. The impact of extreme weather events and fecal indicator bacteria: implications for persistence and transport in the
on the seagrass Zostera noltii and related Hydrobia ulvae population. Mar. Pollut. Neuse River Estuary, North Carolina, USA. Water Res. 42, 941–950.
Bull. 56, 483–492. Froelich, B.A., Williams, T.C., Noble, R.T., Oliver, J.D., 2012. Apparent loss of Vibrio
Carlson, P.R., Yarbro, L.A., Kaufman, K.A., Mattson, R.A., 2010. Vulnerability and vulnificus from North Carolina oysters coincides with drought-induced increase
resilience of seagrasses to hurricane and runoff impacts along Florida’s west in salinity. Appl. Environ. Microbiol. 78, 3885–3889.
coast. Hydrobiologia 649, 39–53. Gibson, C.A., Meyer, J.L., Poff, N.L., Hay, L.E., Georgakakos, A., 2005. Flow regime
Carpenter, S.R., Caraco, N.F., Correll, D.L., Howarth, R.W., Sharpley, A.N., Smith, V.H., alterations under changing climate in two river basins: implications for
1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol. freshwater ecosystems. River Res. Appl. 21, 849–864.
Appl. 8, 559–568. Gillson, J., 2011. Freshwater flow and fisheries production in estuarine and coastal
Chigbu, P., Gordon, S., Strange, T., 2004. Influence of inter-annual variations in systems: where a drop of rain is not lost. Rev. Fish. Sci. 19, 168–186.
climatic factors on fecal coliform levels in Mississippi Sound. Water Res. 38, Hagy, J.D., Lehrter, J.C., Murrell, M.C., 2006. Effects of Hurricane Ivan on water
4341–4352. quality in Pensacola Bay, Florida. Estuar. Coasts 29, 919–925.
Christensen, J.H. et al., 2007. Regional climate projections. In: Solomon, S. et al. Hall, N.S., Litaker, R.W., Fensin, E., Adolf, J.E., Bowers, H.A., Place, A.R., Paerl, H.W.,
(Eds.), Climate Change 2007: The Physical Science Basis. Contribution of 2008. Environmental factors contributing to the development and demise of a
Working Group I to the Fourth Assessment Report of the Intergovernmental toxic dinoflagellate (Karlodinium veneficum) bloom in a shallow, eutrophic,
Panel on Climate Change. Cambridge University Press. lagoonal estuary. Estuar. Coasts 31, 402–418.
CIESIN, 2012. Center for International Earth Science Information Network (CIESIN). Handler, N.B., Paytan, A., Higgins, C.P., Luthy, R.G., Boehm, A.B., 2006. Human
<http://sedac.ciesin.columbia.edu>. development is linked to multiple water body impairments along the California
Cloern, J.E., Alpine, A.E., Cole, B.E., Wong, R.L.J., Arthur, J.F., Ball, M.D., 1983. River coast. Estuar. Coasts 29, 860–870.
discharge controls phytoplankton dynamics in the Northern San Francisco Bay Hickel, W., Mangelsdorf, P., Berg, J., 1993. The human impact in the German Bight –
estuary. Estuar. Coast. Shelf Sci. 16, 415–429. eutrophication during 3 decades (1962–1991). Helgolander Meeresuntersuchungen
Cloern, J.E., 2001. Our evolving conceptual model of the coastal eutrophication 47, 243–263.
problem. Mar. Ecol. Prog. Ser. 210, 223–253. Hobbie, J.E., 2000. Estuarine Sciences—A Synthetic Approach to Research and
Cloern, J.E., Jassby, A.D., Thompson, J.K., Hieb, K.A., 2007. A cold phase of the East Practice. Island Press.
Pacific triggers new phytoplankton blooms in San Francisco Bay. Proc. Natl. Holland, A.F., Sanger, D.M., Gawle, C.P., Lerberg, S.B., Santiago, M.S., Riekerk, G.H.M.,
Acad. Sci. USA 104, 18561–18565. Zimmerman, L.E., Scott, G.I., 2004. Linkages between tidal creek ecosystems and
Conmy, R.N., Coble, P.G., del Castillo, C.E., 2004. Calibration and performance of a the landscape and demographic attributes of their watersheds. J. Exp. Mar. Biol.
new in situ multi-channel fluorometer for measurement of colored dissolved Ecol. 298, 151–178.
organic matter in the ocean. Continent. Shelf Res. 24, 431–442. Hopkinson, C.S., Vallino, J.J., 1995. The relationships among man’s activities in
Cook, P.L.M., Holland, D.P., Longmore, A.R., 2010. Effect of a flood event on the watersheds and estuaries – a model of runoff effects on patterns of estuarine
dynamics of phytoplankton and biogeochemistry in a large temperate community metabolism. Estuaries 18, 598–621.
Australian lagoon. Limnol. Oceanogr. 55, 1123–1133. Hopkinson, C.S., Lugo, A.E., Alber, M., Covich, A.P., Van Bloem, S.J., 2008. Forecasting
Copeland, B.J., 1966. Effects of decreased river flow on estuarine ecology. J. Water effects of sea-level rise and windstorms on coastal and inland ecosystems.
Pollut. Control Fed. 38, 1831–1839. Front. Ecol. Environ. 6, 255–263.
Correll, D.L., Jordan, T.E., Weller, D.E., 1999. Transport of nitrogen and phosphorus Howarth, R.W., Fruci, J.R., Sherman, D., 1991. Inputs of sediment and carbon to an
from Rhode River watersheds during storm events. Water Resour. Res. 35, estuarine ecosystem – influence of land-use. Ecol. Appl. 1, 27–39.
2513–2521. Howarth, R.W., Swaney, D.P., Butler, T.J., Marino, R., 2000. Climatic control on
Costanza, R., d’Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., eutrophication of the Hudson River Estuary. Ecosystems 3, 210–215.
Naeem, S., O’Neill, R.V., Paruelo, J., Raskin, R.G., Sutton, P., van den Belt, M., 1997. Hsieh, J.L., Fries, J.S., Noble, R.T., 2008. Dynamics and predictive modeling of Vibrio
The value of the world’s ecosystem services and natural capital. Nature 387, spp. in the Neuse River Estuary, North Carolina, USA. Environ. Microbiol. 10,
253–260. 57–64.
Coulliette, A.D., Noble, R.T., 2008. Impacts of rainfall on the water quality of the Jannasch, H.W., Coletti, L.J., Johnson, K.S., Fitzwater, S.E., Needoba, J.A., Plant, J.N.,
Newport River Estuary (Eastern North Carolina, USA). J. Water Health 6, 473–482. 2008. The Land/Ocean Biogeochemical Observatory: a robust networked
Cowan, J.L.W., Boynton, W.R., 1996. Sediment–water oxygen and nutrient mooring system for continuously monitoring complex biogeochemical cycles
exchanges along the longitudinal axis of Chesapeake Bay: seasonal patterns, in estuaries. Limnol. Oceanogr. 6, 263–276.
controlling factors and ecological significance. Estuaries 19, 562–580. Jeong, H.J., 2011. Mixotrophy in red tide algae Raphiodphytes. J. Euk. Microbiol. 58,
Cronin, T., Willard, D., Karlsen, A., Ishman, S., Verardo, S., McGeehin, J., Kerhin, R., 215–222.
Holmes, C., Colman, S., Zimmerman, A., 2000. Climatic variability in the eastern Johnk, K.D., Huisman, J., Sharples, J., Sommeijer, B., Visser, P.M., Stroom, J.M., 2008.
United States over the past millennium from Chesapeake Bay sediments. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change
Geology 28, 3–6. Biol. 14, 495–512.
Cronin, T.M., Vann, C.D., 2003. The sedimentary record of climatic and Jordan, T.E., Weller, D.E., Correll, D.L., 2003. Sources of nutrient inputs to the
anthropogenic influence on the Patuxent Estuary and Chesapeake Bay Patuxent River estuary. Estuaries 26, 226–243.
ecosystems. Estuaries 26, 196–209. Kaoru, Y., 1995. Measuring marine recreation benefits of water quality
De Jonge, V.N., Elliott, M., Brauer, V.S., 2006. Marine monitoring: its shortcomings improvements by the nested random utility model. Resour. Energy Econ. 17,
and mismatch with the EU water framework directive’s objective. Mar. Pollut. 119–136.
Bull. 53, 5–19. Kaushal, S.S., Groffman, P.M., Band, L.E., Shields, C.A., Morgan, R.P., Palmer, M.A.,
DeLaune, R., White, J., 2012. Will coastal wetlands continue to sequester carbon in Belt, K.T., Swan, C.M., Findlay, S.E.G., Fisher, G.T., 2008. Interaction between
response to an increase in global sea level? A case study of the rapidly subsiding urbanization and climate variability amplifies watershed nitrate export in
Mississippi River deltaic plain. Clim. Change 110, 297–314. Maryland. Environ. Sci. Technol. 42, 5872–5878.
DiDonato, G.T., Stewart, J.R., Sanger, D.M., Robinson, B.J., Thompson, B.C., Holland, Kempton, J., Keppler, C.J., Lewitus, A., Shuler, A., Wilde, S., 2008. A novel Heterosigma
A.F., van Dolah, R.F., 2009. Effects of changing land use on the microbial water akashiwo (Raphidophyceae) bloom extending from a South Carolina bay to
quality of tidal creeks. Mar. Pollut. Bull. 58, 97–106. offshore waters. Harmful Algae 7, 235–240.
Dix, N.G., Phlips, E.J., Gleeson, R.A., 2008. Water quality changes in the Guana Kendall, M.S., Battista, T., Hillis-Starr, Z., 2004. Long term expansion of a deep
Tolomato Matanzas National Estuarine Research Reserve, Florida, associated Syringodium filiforme meadow in St. Croix, US Virgin Islands: the potential role
with four tropical storms. J. Coast. Res. 55, 26–37. of hurricanes in the dispersal of seeds. Aquat. Bot. 78, 15–25.
Kimmel, D.G., Miller, W.D., Harding, L.W., Houde, E.D., Roman, M.R., 2009. Estuarine Monbet, Y., 1992. Control of phytoplankton biomass in estuaries – a comparative
ecosystem response captured using a synoptic climatology. Estuar. Coasts 32, analysis of microtidal and macrotidal estuaries. Estuaries 15, 563–571.
403–409. Montagna, P.A., Gibeaut, J.C., Tunnell Jr., J.W., 2007. South Texas climate 2100:
Kimmerer, W.J., 2002. Effects of freshwater flow on abundance of estuarine coastal impacts. In: Norwine, J., John, K. (Eds.), South Texas Climate 2100:
organisms: physical effects or trophic linkages? Mar. Ecol. Prog. Ser. 243, 39–55. Problems and Prospects, Impacts and Implications. CREST-RESSACA, Texas A&M
Knutson, T.R., Mcbride, J.L., Chan, J., Emanuel, K., Holland, G., Landsea, C., Held, I., University-Kingsville, Kingsville, Texas, pp. 57–77.
Kossin, J.P., Srivastava, K., Sugi, M., 2010. Tropical cyclones and climate change. Motes, M.L., DePaola, A., Cook, D.W., Veazey, J.E., Hunsucker, J.C., Garthright, W.E.,
Nat. Geosci. 3, 157–163. Blodgett, R.J., Chirtel, S.J., 1998. Influence of water temperature and salinity on
Koch, E.W. et al., 2009. Non-linearity in ecosystem services: temporal and spatial Vibrio vulnificus in northern Gulf and Atlantic Coast oysters (Crassostrea
variability in coastal protection. Front. Ecol. Environ. 7, 29–37. virginica). Appl. Environ. Microbiol. 64, 1459–1465.
Kowalewski, M., Serrano, G.E., Flessa, K.W., Goodfriend, G.A., 2000. Dead delta’s Mulholland, M.R., Morse, R.E., Boneillo, G.E., Bernhardt, P.W., Filippino, K.C., Procise,
former productivity: two trillion shells at the mouth of the Colorado River. L.A., Blanco-Garcia, J.L., Marshall, H.G., Egerton, T.A., Hunley, W.S., Moore, K.A.,
Geology 28, 1059–1062. Berry, D.L., Gobler, C.J., 2009. Understanding causes and impacts of the
Krause-Jensen, D., Middelboe, A.L., Carstensen, J., Dahl, K., 2007. Spatial patterns of dinoflagellate, Cochlodinium polykrikoides, blooms in the Chesapeake Bay.
macroalgal abundance in relation to eutrophication. Mar. Biol. 152, 25–36. Estuar. Coasts 32, 734–747.
Lara, R.J., Neogi, S.B., Islam, M.S., Mahmud, Z.H., Yamasaki, S., Nair, G.B., 2009. Murrell, M.C., Hagy, J.D., Lores, E.M., Greene, R.M., 2007. Phytoplankton production
Influence of catastrophic climate events and human waste on Vibrio distribution and nutrient distributions in a subtropical estuary: importance of freshwater
in the Karnaphuli Estuary, Bangladesh. Ecohealth 6, 279–286. flow. Estuar. Coasts 30, 390–402.
Leggett, C.G., Bockstael, N.E., 2000. Evidence of the effects of water quality on Murrell, M.C., Campbell, J.G., Hagy, J.D., Caffrey, J.M., 2009. Effects of irradiance on
residential land prices. J. Environ. Econ. Manage. 39, 121–144. benthic and water column processes in a Gulf of Mexico estuary: Pensacola Bay,
Lin, J., Xu, H., Cudaback, C., Wang, D., 2008. Inter-annual variability of hypoxic Florida, USA. Estuar. Coast. Shelf Sci. 81, 501–512.
conditions in a shallow estuary. J. Mar. Syst. 73, 169–184. Najjar, R.G., Pyke, C.R., Adams, M.B., Breitburg, D., Hershner, C., Kemp, M., Howarth,
Lindemayer, D.B., Likens, G.E., Franklin, J.F., 2010. Rapid responses to facilitate R., Mulholland, M.R., Paolisso, M., Secor, D., Sellner, K., Waldrop, D., Wood, R.,
ecological discoveries from major disturbances. Front. Ecol. Environ. 8, 527– 2010. Potential climate-change impacts on the Chesapeake Bay. Estuar. Coast.
532. Shelf Sci. 86, 1–20.
Lipp, E.K., Kurz, R., Vincent, R., Rodriguez-Palacios, C., Farrah, S.R., Rose, J.B., 2001. Nixon, S.W., 2003. Replacing the Nile: are anthropogenic nutrients providing the
The effects of seasonal variability and weather on microbial fecal pollution and fertility once brought to the Mediterranean by a great river? Ambio 32, 30–39.
enteric pathogens in a subtropical estuary. Estuaries 24, 266–276. Paerl, H.W., Pinckney, J.L., Fear, J.M., Peierls, B.L., 1998. Ecosystem responses to
Livingston, R.J., Niu, X.F., Lewis, F.G., Woodsum, G.C., 1997. Freshwater input to a internal and watershed organic matter loading: consequences for hypoxia in
gulf estuary: long-term control of trophic organization. Ecol. Appl. 7, 277–299. the eutrophying Neuse River Estuary, North Carolina, USA. Mar. Ecol. Prog. Ser.
Livingston, R.J., Lewis, F.G., Woodsum, G.C., Niu, X.F., Galperin, B., Huang, W., 166, 17–25.
Christensen, J.D., Monaco, M.E., Battista, T.A., Klein, C.J., Howell, R.L., Ray, G.L., Paerl, H.W., Bales, J.D., Ausley, L.W., Buzzelli, C.P., Crowder, L.B., Eby, L.A., Fear, J.M.,
2000. Modelling oyster population response to variation in freshwater input. Go, M., Peierls, B.L., Richardson, T.L., Ramus, J.S., 2001. Ecosystem impacts of
Estuar. Coast. Shelf Sci. 50, 655–672. three sequential hurricanes (Dennis, Floyd, and Irene) on the United States’
Longstaff, B.J., Dennison, W.C., 1999. Seagrass survival during pulsed turbidity largest lagoonal estuary, Pamlico Sound, NC. Proc. Natl. Acad. Sci. 98, 5655–
events: the effects of light deprivation on the seagrasses Halodule pinifolia and 5660.
Halophila ovalis. Aquat. Bot. 65, 105–121. Paerl, H.W., Valdes, L.M., Peierls, B.L., Adolf, J.E., Harding, L.W., 2006. Anthropogenic
Magnien, R.E., Summers, R.M., Sellner, K.G., 1992. External nutrient sources, internal and climatic influences on the eutrophication of large estuarine ecosystems.
nutrient pools, and phytoplankton production in Chesapeake Bay. Estuaries 15, Limnol. Oceanogr. 51, 448–462.
497–516. Paerl, H.W., Hall, N.S., Calandrino, E.S., 2011. Controlling harmful cyanobacterial
Mallin, M.A., Posey, M.H., Shank, G.C., McIver, M.R., Ensign, S.H., Alphin, T.D., 1999. blooms in a world experiencing anthropogenic and climatic-induced change.
Hurricane effects on water quality and benthos in the Cape Fear watershed: Sci. Total Environ. 409, 1739–1745.
natural and anthropogenic impacts. Ecol. Appl. 9, 350–362. Pall, P., Aina, T., Stone, D.A., Stott, P.A., Nozawa, T., Hilberts, A.G.J., Lohmann, D.,
Mallin, M.A., Williams, K.E., Esham, E.C., Lowe, R.P., 2000. Effect of human Allen, M.R., 2011. Anthropogenic greenhouse gas contribution to flood risk in
development on bacteriological water quality in coastal watersheds. Ecol. England and Wales in Autumn 2000. Nature 470, 382–386.
Appl. 10, 1047–1056. Palmer, M.A., Liermann, C.A.R., Nilsson, C., Florke, M., Alcamo, J., Lake, P.S., Bond, N.,
Mallin, M.A., Ensign, S.H., McIver, M.R., Shank, G.C., Fowler, P.K., 2001. Demographic, 2008. Climate change and the world’s river basins: anticipating management
landscape, and meteorological factors controlling the microbial pollution of options. Front. Ecol. Environ. 6, 81–89.
coastal waters. Hydrobiologia 460, 185–193. Paz, S., Bisharat, N., Paz, E., Kidar, O., Cohen, D., 2007. Climate change and the
Mallin, M.A., Posey, M.H., McIver, M.R., Parsons, D.C., Ensign, S.H., Alphin, T.D., 2002. emergence of Vibrio vulnificus disease in Israel. Environ. Res. 103, 390–396.
Impacts and recovery from multiple hurricanes in a Piedmont-coastal plain Peierls, B.L., Caraco, N.F., Pace, M.L., Cole, J.J., 1991. Human influence on river
river system. Bioscience 52, 999–1010. nitrogen. Nature 350, 386–387.
Mallin, M.A., Corbett, C.A., 2006. How hurricane attributes determine the extent of Peierls, B.L., Christian, R.R., Paerl, H.W., 2003. Water quality and phytoplankton as
environmental effects: multiple hurricanes and different coastal systems. indicators of hurricane impacts on a large estuarine ecosystem. Estuaries 26,
Estuar. Coasts 29, 1046–1061. 1329–1343.
Mallin, M.A., Johnson, V.L., Ensign, S.H., 2009. Comparative impacts of stormwater Pendleton, L.H., 2008. The Economic and Market Value of Coasts and Estuaries:
runoff on water quality of an urban, a suburban, and a rural stream. Environ. What’s at Stake? Restore America’s Estuaries, 182 p.
Monit. Assess. 159, 475–491. Perissinotto, R., Pillay, D., Bate, G., 2010. Microalgal biomass in the St. Lucia Estuary
Maraun, D. et al., 2010. Precipitation downscaling under climate change: recent during the 2004 to 2007 drought period. Mar. Ecol. Prog. Ser. 405, 147–161.
developments to bridge the gap between dynamical models and the end user. Petes, L.E., Brown, A.J., Knight, C.R., 2012. Impacts of upstream drought and water
Rev. Geophys. 48. http://dx.doi.org/10.1029/2009RG000314. withdrawals on the health and survival of downstream estuarine oyster
Massey, D.M., Newbold, S.C., Gentner, B., 2006. Valuing water quality changes using populations. Ecol. Evol. 2, 1712–1724.
a bioeconomic model of a coastal recreational fishery. J. Environ. Econ. Manage. Pfeffer, C.S., Hite, M.F., Oliver, J.D., 2003. Ecology of Vibrio vulnificus in estuarine
52, 482–500. waters of eastern North Carolina. Appl. Environ. Microbiol. 69, 3526–3531.
McDonald, R.I., Green, P., Balk, D., Fekete, B.M., Revenga, C., Todd, M., Montgomery, Phlips, E.J., Badylak, S., Christman, M.C., Lasi, M.A., 2010. Climatic trends and
M., 2011. Urban growth, climate change, and freshwater availability. Proc. Natl. temporal patterns of phytoplankton composition, abundance, and succession in
Acad. Sci. 108, 6312–6317. the Indian River Lagoon, Florida, USA. Estuar. Coasts 33, 498–512.
McKee, K.L., Mendelssohn, I.A., Materne, M.D., 2004. Acute salt marsh dieback in the Plant, J.N., Johnson, K.S., Needoba, J.A., Coletti, L.J., 2009. NH4–Digiscan: an in situ
Mississippi River deltaic plain: a drought-induced phenomenon? Global Ecol. and laboratory ammonium analyzer for estuarine, coastal, and shelf waters.
Biogeogr. 13, 65–73. Limnol. Oceanogr. Methods 7, 144–156.
Meehl, G.A. et al., 2007. Global climate projections. In: Solomon, S. et al. (Eds.), Pollack, J.B., Palmer, T.A., Montagna, P.A., 2011. Long-term trends in the response of
Climate Change 2007: The Physical Science Basis. Contribution of Working benthic macrofauna to climate variability in the Lavaca-Colorado Estuary,
Group I to the Fourth Assessment Report of the Intergovernmental Panel on Texas. Mar. Ecol. Prog. Ser. 436, 67–80.
Climate Change. Cambridge University Press. Preen, A.R., Long, W.J.L., Coles, R.G., 1995. Flood and cyclone related loss, and partial
Meyer, J.L., Sale, M.J., Mulholland, P.J., Poff, N.L., 1999. Impacts of climate change on recovery, of more than 1000 km2 of seagrass in Hervey-Bay, Queensland,
aquatic ecosystem functioning and health. J. Am. Water Res. Assoc. 35, 1373– Australia. Aquat. Bot. 52, 3–17.
1386. Rabalais, N.N., Turner, R.E., Diaz, R.J., Justic, D., 2009. Global change and
Miller, W.D., Harding, L.W., Adolf, J.E., 2006. Hurricane Isabel generated an unusual eutrophication of coastal waters. ICES J. Mar. Sci. 66, 1528–1537.
fall bloom in Chesapeake Bay. Geophys. Res. Lett. 33, L06612. http://dx.doi.org/ Rask, N., Pederson, S.E., Jensen, M.H., 1999. Response to lowered nutrient discharges
10.1029/2005GL025658. in the coastal waters around the island of Funen, Denmark. Hydrobiologia 393,
Milliman, J.D., Farnsworth, K.L., Jones, P.D., Xu, K.H., Smith, L.C., 2008. Climatic and 69–81.
anthropogenic factors affecting river discharge to the global ocean, 1951–2000. Richardson, T.L., Lawrenz, E., Pinckney, J.L., Guajardo, R.C., Walker, E.A., Paerl, H.W.,
Global Planet. Change 62, 187–194. MacIntyre, H.L., 2010. Spectral fluorometric characterization of phytoplankton
Min, S., Zhang, X., Zwiers, F.W., Hegerl, G.C., 2011. Human contribution to more community composition using the Algae Online Analyser (R). Water Res. 44,
intense precipitation extremes. Nature 470, 378–381. 2461–2472.
Rothenberger, M.B., Burkholder, J.M., Brownie, C., 2009. Long-term effects of van Dolah, R.F., Riekerk, G.H.M., Bergquist, D.C., Felber, J., Chestnut, D.E., Holland,
changing land use practices on surface water quality in a coastal river and A.F., 2008. Estuarine habitat quality reflects urbanization at large spatial scales
lagoonal estuary. Environ. Manage. 44, 505–523. in South Carolina’s coastal zone. Sci. Total Environ. 390, 142–154.
Scavia, D., Field, J.C., Boesch, D.F., Buddemeier, R.W., Burkett, V., Cayan, D.R., Fogarty, van Drecht, G., Bouwman, A.F., Harrison, J., Knoop, J.M., 2009. Global nitrogen and
M., Harwell, M.A., Howarth, R.W., Mason, C., Reed, D.J., Royer, T.C., Sallenger, phosphate in urban wastewater for the period 1970 to 2050. Global
A.H., Titus, J.G., 2002. Climate change impacts on U.S. coastal and marine Biogeochem. Cycles 23. http://dx.doi.org/10.1029/2009GB003458.
ecosystems. Estuaries 25, 149–164. Vernberg, F.J., Vernberg, W.B., Blood, E., Fortner, A., Fulton, M., McKellar, H.,
Schallenberg, M., Larned, S.T., Hayward, S., Arbuckle, C., 2010. Contrasting effects of Michener, W., Scott, G., Siewicki, T., Elfigi, K., 1992. Impact of urbanization on
managed opening regimes on water quality in two intermittently closed and high-salinity estuaries in the southeastern United States. Neth. J. Sea Res. 30,
open coastal lakes. Estuar. Coast. Shelf Sci. 86, 587–597. 239–248.
Schiermeier, Q., 2010. The real holes in climate science. Nature 463, 284–287. Vorosmarty, C.J., Green, P., Salisbury, J., Lammers, R.B., 2000. Global water
Sigleo, A.C., Frick, W.E., 2007. Seasonal variations in river discharge and nutrient resources: vulnerability from climate change and population growth. Science
export to a Northeastern Pacific estuary. Estuar. Coast. Shelf Sci. 73, 368– 289, 284–288.
378. Voynova, Y.G., Sharp, J.H., 2012. Anomalous biogeochemical response to a flooding
Stahle, D.W., Cleaveland, M.K., Hehr, J.G., 1988. North Carolina climate changes event in the Delaware Estuary: a possible typology shift due to climate change.
reconstructed from tree rings: A.D. 372 to 1985. Science 240, 1517–1519. Estuar. Coasts 35, 943–958.
Stanley, D.W., Nixon, S.W., 1992. Stratification and bottom-water hypoxia in the Waycott, M. et al., 2009. Accelerating loss of seagrasses across the globe threatens
Pamlico River estuary. Estuaries 15, 270–281. coastal ecosystems. Proc. Natl. Acad. Sci. USA 106, 12377–12381.
Steward, J.S., Virnstein, R.W., Lasi, M.A., Morris, L.J., Miller, J.D., Hall, L.M., Tweedale, Weiskel, P.K., Howes, B.L., Heufelder, G.R., 1996. Coliform contamination of a coastal
W.A., 2006. The impacts of the 2004 hurricanes on hydrology, water quality, embayment: sources and transport pathways. Environ. Sci. Technol. 30, 1872–
and seagrass in the central Indian River Lagoon, Florida. Estuar. Coasts 29, 954– 1881.
965. Wetz, J.J., Blackwood, A.D., Fries, J.S., Williams, Z.F., Noble, R.T., 2008. Trends in total
Stutes, A.L., Cebrian, J., Corcoran, A.A., 2006. Effects of nutrient enrichment and Vibrio spp. and Vibrio vulnificus concentrations in the eutrophic Neuse River
shading on sediment primary production and metabolism in eutrophic Estuary, North Carolina, during storm events. Aquat. Microb. Ecol. 53, 141–149.
estuaries. Mar. Ecol. Prog. Ser. 312, 29–43. Wetz, M.S., Paerl, H.W., 2008. Estuarine phytoplankton responses to hurricanes and
Taljaard, S., Snow, G., Gama, P., van Niekerk, L., 2009. Verification of a conceptual tropical storms with different characteristics (trajectory, rainfall, winds). Estuar.
model of water quality for small temporarily open/closed estuaries: East Coasts 31, 419–429.
Kleinemonde Estuary, South Africa. Mar. Freshwater Res. 60, 234–245. Wetz, M.S., Hutchinson, E., Lunetta, R., Paerl, H.W., Taylor, J.C., 2011. Severe
Tomasko, D.A., Anastasiou, C., Kovach, C., 2006. Dissolved oxygen dynamics in droughts reduce planktonic production in estuaries with cascading effects on
Charlotte Harbor and its contributing watershed, in response to Hurricanes higher trophic levels. Limnol. Oceanogr. 56, 627–638.
Charley, Frances, and Jeanne – impacts and recovery. Estuar. Coasts 29, 932– Williams, C.J., Boyer, J.N., Jochem, F.J., 2008. Indirect hurricane effects on resource
938. availability and microbial communities in a subtropical wetland-estuary
Trenberth, K.E., Fasullo, J.T., 2012. Climate extremes and climate change: the transition zone. Estuar. Coasts 31, 204–214.
Russian heat wave and other climate extremes of 2010. J. Geophys. Res. Atmos. Wong, V.N.L., Johnston, S.G., Bush, R.T., Sullivan, L.A., Clay, C., Burton, E.G., Slavich,
117. http://dx.doi.org/10.1029/2012JD018020. P.G., 2010. Spatial and temporal changes in estuarine water quality during a
Trenberth, K.E., 2012. Framing the way to relate climate extremes to climate post-flood hypoxic event. Estuar. Coast. Shelf Sci. 87, 73–82.
change. Clim. Change 115, 283–290. Yoskowitz, D., Santos, C., Allee, B., Carollo, C., Henderson, J., Jordan, S., Ritchie, J.,
United Nations, 2011. World Population Prospects: The 2010 Revision, Highlights, 2010. Proceedings of the Gulf of Mexico Ecosystem Services Workshop: Bay St.
and Advance Tables. 164 p. Louis, Mississippi, June 16–18, 2010. 16 p. Harte Research Institute for Gulf of
Valiela, I., Peckol, P., D’Avanzo, C., Kremer, J., Hersh, D., Foreman, K., Lajtha, K., Seely, Mexico Studies.
B., Geyer, W.R., Isaji, T., Crawford, R., 1998. Ecological effects of major storms on Yoon, B., Raymond, P.A., 2012. Dissolved organic matter export from a forested
coastal watersheds and coastal waters: hurricane Bob on Cape Cod. J. Coast. Res. watershed during Hurricane Irene. Geophys. Res. Lett. 39. http://dx.doi.org/
14, 218–238. 10.1029/2012GL052785.

An - Extreme - Future - For - Estuaries - Effects - Wetz 2013

Uploaded by

Copyright:

Available Formats

An - Extreme - Future - For - Estuaries - Effects - Wetz 2013

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

An - Extreme - Future - For - Estuaries - Effects - Wetz 2013

Uploaded by

Copyright:

Available Formats

Marine Pollution Bulletin 69 (2013) 7–18

Contents lists available at SciVerse ScienceDirect

Marine Pollution Bulletin

An ‘extreme’ future for estuaries? Effects of extreme climatic events

ecological effects of ECE on the coastal zone, our knowledge is lim-

1. How do ECE affect estuarine water quality, and does this

These questions must be answered to effectively project and

2. Effects of extreme climatic events on estuarine water quality

2.1.1. Tropical cyclones and floods

events, can create conditions that are unfavorable for phytoplank-

DIN Anomaly (µM) Flow anomaly (m³ s-¹)

Chl Anomaly (µg L-1)

Water quality indicator Short-term (days– Long-term (months–

You might also like