ArticlePDF Available

Recent increases of rainfall and flooding from tropical cyclones (TCs) in North Carolina (USA): implications for organic matter and nutrient cycling in coastal watersheds

Authors:

Abstract and Figures

Coastal North Carolina experienced 36 tropical cyclones (TCs), including three floods of historical significance in the past two decades (Hurricanes Floyd-1999, Matthew-2016 and Florence-2018). These events caused catastrophic flooding and major alterations of water quality, fisheries habitat and ecological conditions of the Albemarle-Pamlico Sound (APS), the second largest estuarine complex in the United States. Continuous rainfall records for coastal NC since 1898 reveal a period of unprecedented high precipitation storm events since the late-1990s. Six of seven of the “wettest” storm events in this > 120-year record occurred in the past two decades, identifying a period of elevated precipitation and flooding associated with recent TCs. We examined storm-related freshwater discharge, carbon (C) and nutrient, i.e., nitrogen (N) and phosphorus (P) loadings, and evaluated contributions to total annual inputs in the Neuse River Estuary (NRE), a major sub-estuary of the APS. These contributions were highly significant, accounting for > 50% of annual loads depending on antecedent conditions and storm-related flooding. Depending on the magnitude of freshwater discharge, the NRE either acted as a “processor” to partially assimilate and metabolize the loads or acted as a “pipeline” to transport the loads to the APS and coastal Atlantic Ocean. Under base-flow, terrestrial sources dominate riverine carbon. During storm events these carbon sources are enhanced through the inundation and release of carbon from wetlands. These findings show that event-scale discharge plays an important and, at times, predominant role in C, N and P loadings. We appear to have entered a new climatic regime characterized by more frequent extreme precipitation events, with major ramifications for hydrology, cycling of C, N and P, water quality and habitat conditions in estuarine and coastal waters.
Content may be subject to copyright.
Recent increases of rainfall and flooding from tropical
cyclones (TCs) in North Carolina (USA): implications
for organic matter and nutrient cycling in coastal
watersheds
Hans W. Paerl .Nathan S. Hall .Alexandria G. Hounshell .Karen L. Rossignol .
Malcolm A. Barnard .Richard A. Luettich Jr. .Jacob C. Rudolph .
Christopher L. Osburn .Jerad Bales .Lawrence W. Harding Jr.
Received: 4 April 2020 / Accepted: 28 July 2020 / Published online: 11 August 2020
ÓSpringer Nature Switzerland AG 2020
Abstract Coastal North Carolina experienced 36
tropical cyclones (TCs), including three floods of
historical significance in the past two decades (Hur-
ricanes Floyd-1999, Matthew-2016 and Florence-
2018). These events caused catastrophic flooding
and major alterations of water quality, fisheries habitat
and ecological conditions of the Albemarle-Pamlico
Sound (APS), the second largest estuarine complex in
the United States. Continuous rainfall records for
coastal NC since 1898 reveal a period of unprece-
dented high precipitation storm events since the late-
1990s. Six of seven of the ‘‘wettest’’ storm events in
this [120-year record occurred in the past two
decades, identifying a period of elevated precipitation
and flooding associated with recent TCs. We exam-
ined storm-related freshwater discharge, carbon
(C) and nutrient, i.e., nitrogen (N) and phosphorus
(P) loadings, and evaluated contributions to total
annual inputs in the Neuse River Estuary (NRE), a
major sub-estuary of the APS. These contributions
were highly significant, accounting for [50% of
annual loads depending on antecedent conditions and
storm-related flooding. Depending on the magnitude
of freshwater discharge, the NRE either acted as a
‘processor’’ to partially assimilate and metabolize the
loads or acted as a ‘‘pipeline’’ to transport the loads to
the APS and coastal Atlantic Ocean. Under base-flow,
terrestrial sources dominate riverine carbon. During
storm events these carbon sources are enhanced
through the inundation and release of carbon from
wetlands. These findings show that event-scale dis-
charge plays an important and, at times, predominant
Responsible Editor: James Sickman.
H. W. Paerl (&)N. S. Hall K. L. Rossignol
M. A. Barnard R. A. Luettich Jr.
Institute of Marine Sciences, University of North Carolina
at Chapel Hill, Morehead City, NC 28557, USA
e-mail: hpaerl@email.unc.edu
A. G. Hounshell
Department of Biological Sciences, Virginia Tech,
Blacksburg, VA 24061, USA
J. C. Rudolph C. L. Osburn
Department of Marine, Earth and Atmospheric Sciences,
North Carolina State University, Raleigh,
NC 27607, USA
J. Bales
Consortium of Universities for the Advancement of
Hydrologic Science, Cambridge, MA 02140, USA
L. W. Harding Jr.
Department of Atmospheric and Oceanic Sciences,
University of California, Los Angeles, Los Angeles,
CA 90095, USA
123
Biogeochemistry (2020) 150:197–216
https://doi.org/10.1007/s10533-020-00693-4(0123456789().,-volV)(0123456789().,-volV)
role in C, N and P loadings. We appear to have entered
a new climatic regime characterized by more frequent
extreme precipitation events, with major ramifications
for hydrology, cycling of C, N and P, water quality and
habitat conditions in estuarine and coastal waters.
Keywords Tropical cyclones Flooding Organic
carbon Nutrient cycling Phytoplankton Estuarine
Coastal North carolina
Introduction
Since the mid-1990s, coastal North Carolina, USA has
been struck by 36 tropical cyclones (TCs), indicative
of a recent increase in such events (Paerl et al.
2018,2019) (Fig. 1and Table 1). This increase
appears to reflect regional and global patterns, as the
frequency and magnitude of events have increased
over several decades (Webster et al. 2005; Holland
and Webster 2007; Seneviratne et al. 2012; Wuebbles
et al. 2014; NOAA National Hurricane Center-Fig. 2).
North Carolina’s low-lying, readily flooded coastal
region is on the ‘‘front doorstep’’ of these increases
with concomitant biogeochemical and trophic impacts
(Frankson et al. 2019). The number of TCs making
landfall in North Carolina is highly variable from year
to year, while TC intensity and rainfall rates are
projected to increase in a warming climate (Konrad
and Perry 2010). This low-lying region is also
impacted by sea level rise (Frankson et al. 2019),
which combines with frequent TCs to make coastal
North Carolina and the neighboring mid-Atlantic
region highly vulnerable to flooding.
In the last two decades (1999–2019), coastal North
Carolina experienced three major floods from TCs that
were considered 50-year events (i.e., an annual
probability of 2%): Floyd (1999), Matthew (2016),
and Florence (2018) (Paerl et al. 2019). An examina-
tion of major storm events impacting the North
Carolina coastline since 1898 indicated that 6 of 7 of
the highest rainfall events occurred during the last two
decades (Paerl et al. 2019), a trend in keeping with
increased precipitation associated with TCs globally
(Allan and Soden 2008; Asadieh and Krakauer 2015;
Lehmann et al. 2015). These storms led to unprece-
dented flood damage, accompanied by large inorganic
and organic C, N and P pulses in freshwater discharge
impacting estuarine and coastal waters (Bianchi et al.
Fig. 1 Tropical cyclone dates and tracks as they impacted coastal North Carolina, USA, since the recent period of elevated storm
activity which commenced in the mid-1990s. Updated from Paerl et al. (2018)
123
198 Biogeochemistry (2020) 150:197–216
Table 1 Tropical cyclones impacting North Carolina from 1996–2019
Tropical cyclone Date Storm characteristics
(Paerl et al. 2018)
Precipitation
amount (mm)
Impact on
North Carolina
Tropical Storm Arthur 20 Jun 1996 Dry and windy 100 Moderate
Hurricane Bertha 12 Jul 1996 Dry and windy 80 Moderate
Hurricane Fran 6 Sep 1996 Wet and windy 406 Major
Tropical Storm Josephine 8 Oct 1996 Wet and windy 100 Moderate
Hurricane Danny 24 Jul 1997 Dry and calm 300 Minimal
Hurricane Bonnie 27 Aug 1998 Dry and windy 371 Major
Hurricane Earl 4 Sep 1998 Dry and windy 102 Moderate
Hurricane Dennis 4 Sep 1999 Wet and windy 506 Major
Hurricane Floyd 16 Sep 1999 Wet and windy 484 Major
Hurricane Irene 18 Oct 1999 Wet and windy 255 Major
Hurricane Gordon 19 Sep 2000 Wet and windy 145 Major
Tropical Storm Helene 23 Sep 2000 Dry and windy 211 Moderate
Tropical Storm Allison 13 Jun 2001 Dry and calm 406 Moderate
Hurricane Gustav 10 Sep 2002 Dry and windy 125 Minimal
Hurricane Isabel 18 Sep 2003 Dry and windy 115 Moderate
Hurricane Alex 3 Aug 2004 Dry and calm 127 Minimal
Tropical Storm Bonnie 13 Aug 2004 Dry and calm 77 Minimal
Hurricane Charley 14 Aug 2004 Wet and calm 150 Minimal
Hurricane Gaston 30 Aug 2004 Dry and calm 155 Minimal
Hurricane Ophelia 14 Sep 2005 Dry and windy 254 Major
Hurricane Ernesto 1 Aug 2006 Wet and windy 371 Major
Tropical Storm Barry 3 Jun 2007 Dry and windy 95 Minimal
Tropical Storm Gabrielle 9 Sep 2007 Dry and calm 200 Minimal
Tropical Storm Cristobal 20 Jul 2008 Dry and calm 87 Minimal
Hurricane Hanna 29 Sep 2008 Dry and calm 97 Minimal
Hurricane Earl 3 Sep 2010 Dry and windy 115 Moderate
Hurricane Nicole 29 Sep 2010 Wet and calm 573 Major
Hurricane Irene 27 Aug 2011 Wet and windy 360 Major
Tropical Storm Beryl 30 May 2012 Dry and windy 179 Minimal
Tropical Storm Andrea 7 Jun 2013 Dry and windy 188 Minimal
Hurricane Arthur 4 Jul 2014 Dry and windy 107 Moderate
Tropical Storm Ana 7 May 2015 Wet and calm 175 Minimal
Hurricane Joaquin 3 Oct 2015 Wet and windy 200 Major
Hurricane Hermine 2 Sep 2016 Dry and windy 200 Minimal
Hurricane Matthew 8 Oct 2016 Wet and windy 610 Major
Hurricane Florence 14 Sep 2018 Wet and Windy 913 Major
Hurricane Michael 11 Oct 2018 Wet and calm 330 Moderate
Hurricane Dorian 5 Sep 2019 Wet and Calm 250 Moderate
The tropical cyclones are listed with the date of impact in North Carolina, the characteristics of the storm, rainfall amounts in North
Carolina, and the impact on North Carolina
123
Biogeochemistry (2020) 150:197–216 199
2013; Paerl et al. 2006; Osburn et al. 2019a,b)
(Fig. 3). Increasingly frequent extreme events in
recent years appear to be altering hydrologic and
biogeochemical dynamics of estuarine and coastal
waters, leading us to pose the question: Are we
witnessing increasing occurrences of ‘‘hot moments’
that ‘‘occur when episodic hydrological flow-paths
reactivate and/or mobilize accumulated reactants?’’
(McClain et al. 2003).
In this contribution, we draw on a long-term water
quality monitoring program (since 1994) to charac-
terize and quantify C, N and P inputs to the nutrient-
sensitive receiving waters of the Neuse River Estuary
(NRE), a major tributary of the 2nd largest estuarine
complex in the United States, and the Albemarle-
Pamlico Sound (APS), the US’s largest lagoonal
ecosystem and a major fisheries nursery. We also
examined hydrologic and nutrient impacts on the base
of the food web in the NRE where phytoplankton
account for [80% of primary production (Paerl et al.
1998). These events also promote hypoxia and anoxia,
which are commonly observed in periodically verti-
cally-stratified sub-estuaries of the APS (Mallin and
Corbett 2006). These impacts have been detailed for
the NRE in previous publications (Paerl et al.
2006,2018).
The objectives of this study were to quantify event-
scale responses to TCs compared to seasonal- to
interannual patterns of C, N and P loadings as baseline
conditions. We addressed two questions: (1) How does
the recent increase of precipitation and freshwater
discharge associated with TCs drive fundamental
changes of C, N and P cycling in the NRE-APS
continuum and adjacent coastal waters, and (2) What
are the overall biogeochemical and ecological impacts
of increased loadings?
Methods and materials
Study site: the Neuse River Estuary-Pamlico
Sound estuarine continuum
North Carolina’s Neuse River Estuary (NRE) is a
lagoonal, micro-tidal ecosystem, representative of *
20 global estuarine and coastal waters (Kennish and
Paerl 2010). It is the largest sub-estuary of the
Albemarle-Pamlico Sound (APS) system. The APS
drains approximately 50% of North Carolina’s and
20% of Virginia’s coastal plain regions via 5 major
rivers (Bales et al. 2000; Bales 2003) (Fig. 4). The
NRE receives inputs from a 14,600 km
2
watershed that
has experienced urbanization of its headwaters and has
intensive, rapidly expanding row-crop agriculture and
swine/poultry operations toward the coast (Stow et al.
2001; Paerl et al. 2019). As for many estuarine and
coastal waters, primary production and algal bloom
formation in the NRE are largely N-limited for much
of the year (Paerl et al. 1995,2007; Rudek et al. 1991).
High water column primary production ([300 g C
m
-2
y
-1
) results from excessive N loading and
efficient recycling, especially in the summer (Chris-
tian et al. 1991; Boyer et al. 1993,1994). Vertical
density stratification in the main channel also pro-
motes extensive bottom-water hypoxia (\2.0 mg O
2
L
-1
) in summer-fall (Buzzelli et al. 2002).
The full sequence of biotic responses to nutrient and
hydrologic perturbations in estuarine and coastal
waters dominated by freshwater discharge may not
fully develop or can be masked by rapid flushing
(Hopkinson and Vallino 1995). However, the APS is
poorly flushed due its large estuarine volume relative
to river inflows, the microtidal regime of the NC
coastline, and weak tidal exchange through three
shallow inlets along the Outer Banks. Residence times
generally range from one to three months for the NRE
and up to a year for Pamlico Sound (Pietrafesa et al.,
1996; Paerl et al. 2009; Peierls et al. 2012) and are
strongly impacted by changes in freshwater input.
Changes in residence time due to floods or droughts
are accompanied by changes in salinity and nutrient
concentrations that drive significant changes in the
Fig. 2 History of the tropical storms, hurricanes, and major
hurricanes (Category 3?) in the North Atlantic Ocean, derived
from the analysis of the National Hurricane Center, Miami, FL,
USA
123
200 Biogeochemistry (2020) 150:197–216
phytoplankton community (Hall et al. 2008; Paerl
et al. 2018). The NRE has been the site of numerous
harmful algal bloom events, ranging from toxic
cyanobacterial blooms upstream (Paerl 1983; Fulton
and Paerl 1988; Lung and Paerl 1988) to dinoflagellate
and raphidophyte blooms downstream (Pinckney et al.
1997,1998; Valdes-Weaver et al. 2006; Paerl et al.
2007,2010,2013; Hall et al. 2008).
The Neuse River Estuary Modeling and Monitoring
Program (ModMon) (https://paerllab.web.unc.edu/
projects/modmon/) has produced a database of
observational, experimental research, and modeling
results on C dynamics, nutrient-productivity relation-
ships, and algal blooms (Luettich et al. 2000; Bowen
and Hieronymus 2000; Paerl et al. 2009; Peierls et al.
2012) for the Neuse River Estuary since 1994 and for
western Pamlico Sound (PS) since 2000. Other
observations are provided by the North Carolina
Department of Environmental Quality (NC-DEQ),
which conducts monthly water-quality monitoring
(including phytoplankton taxonomic composition) in
the NRE. Together, these activities comprise more
than 25 years of data with high spatio-temporal reso-
lution (c.f. Paerl et al. 2018).
Fig. 3 US Geological Survey’s Landsat 8 satellite showing
colored dissolved organic matter (CDOM) in floodwater
discharged to North Carolina estuarine and coastal ecosystems
following Hurricane Florence in September, 2018. Upper frame
shows a true color image, while lower frame has been processed
to emphasize CDOM. Photo courtesy of Landsat Data Webpage
(https://www.usgs.gov/land-resources/nli/landsat)
123
Biogeochemistry (2020) 150:197–216 201
ModMon sampling consisted of bi-weekly visits to
11 stations along the main axis of the NRE (Fig. 3),
including vertical profiles with collection of near-
surface and near-bottom water (Paerl 2005; Paerl et al.
2006). In western PS, samples were collected monthly
at nine stations (Fig. 4). At each station, profiles of
temperature, salinity, and dissolved oxygen were
made at 0.5 m depth intervals using a YSI 6600
multi-parameter water quality sonde (Yellow Springs
Inc, Yellow Springs, OH). Dissolved oxygen was
calibrated with water-saturated air according to the
YSI User’s Manual with accuracy of 2% or 0.2 mg
L
-1
. Discrete samples for nutrient concentrations,
phytoplankton biomass and community composition,
and inorganic and organic C species were collected
from near-surface (0.2 m depth) and bottom waters
(0.5 m above bottom) using a non-destructive dia-
phragm pump, dispensed into 4 L polyethylene
bottles. Samples were maintained in the dark at
in situ temperature in a large insulated container and
returned to the laboratory at the UNC-CH Institute of
Marine Sciences, Morehead City (IMS) within 4 h of
collection for processing.
Freshwater discharge, flushing time, C and nutrient
loading
Average, daily discharge from the Neuse River was
measured by the US Geological Survey at Fort
Barnwell (USGS 02091814) (Fig. 4). Daily material
loadings of C, N and P were calculated using
Weighted Regressions on Time Discharge and Season
(WRTDS) (Hirsch and DeCicco 2015; Hirsch et al.
2010) using daily average river flow and material
concentrations at the head of the estuary by ModMon
(or NC DEQ for total N and total P) (Fig. 4). Half
window widths of the tricube weight function were set
to default values: 6 months for seasonality, 7 years for
time, and 2 natural log units for discharge (Hirsch and
DeCicco 2015). Changes in flushing time of the Neuse
River Estuary that resulted from changing river flow
conditions were calculated based on freshwater dis-
charge at Fort Barnwell and salinity depth profiles
measured at ModMon stations 0 to 180 using the date-
specific freshwater replacement method (Alber and
Sheldon 1999). See Peierls et al. (2012) for details on
how the method was implemented.
Fig. 4 Maps showing (left) the location of the Neuse River
estuary, its watershed and the downstream Pamlico Sound. The
right hand side shows the Neuse River and its Estuary, including
the upstream Fort Barnwell USGS gaging station and the water
quality sampling stations of the Neuse River Modeling and
Monitoring Program, ModMon. The locations of the EPA Clean
Air Status and Trends Network (CASTNET) air monitoring site
BFT142 and National Data Buoy Center station CLKN7 at Cape
Lookout are also shown
123
202 Biogeochemistry (2020) 150:197–216
Carbon and nutrient analyses
C and N measured at ModMon stations included: total
dissolved nitrogen (TDN), nitrate plus nitrite (NO
3
--
?NO
2
-
), ammonium (NH
4
?
), soluble reactive
phosphate (SRP), dissolved organic carbon (DOC),
dissolved inorganic carbon (DIC), particulate organic
carbon (POC), and particulate nitrogen (PN). Dis-
solved inorganic nitrogen (DIN) was NO
3
-
?NO
2
--
?NH
4
?
. Dissolved organic nitrogen (DON) was
computed by difference as TDN—DIN. Nutrient
analyses used 100 mL aliquots filtered through pre-
combusted (4 h at 525 °C) 25 mm diameter Whatman
GF/F filters into acid-washed and sample-rinsed
150 mL polyethylene bottles that were subsequently
frozen at -20 °C. Filtrates were analyzed for dis-
solved N forms and SRP with a Lachat/Zellweger
Analytics QuickChem 8000 flow injection autoana-
lyzer using standard protocols (Lachat method num-
bers 31-107-04-1-C, 31-107-06-1-B, and 31-115-01-
3-C, respectively) (Peierls et al. 2012). Particulate
organic carbon and nitrogen were measured on seston
collected on pre-combusted GF/F filters, analyzed by
high-temperature combustion using a Costech ECS
4010 analyzer (Peierls and Paerl 2010). DIC and DOC
were measured on a Shimadzu Total Organic Carbon
Analyzer (TOC-5000A) (Crosswell et al. 2014).
Phytoplankton biomass
Chlorophyll a(Chl-a), an indicator of phytoplankton
biomass, was measured on near-surface and near-
bottom samples by filtering 50 mL of NRE water onto
GF/F filters. Filters were frozen at -20 °C and
subsequently extracted using a tissue grinder in 90%
acetone (EPA method 445.0, Arar et al. 1997). Chl-
ain extracts were measured using the non-acidifica-
tion method of Welschmeyer (1994) on a Turner
Designs Trilogy fluorometer calibrated with pure Chl-
a(Turner Designs, Sunnyvale, CA).
Results and discussion
Loads of dissolved organic carbon (DOC), total N
(TN) and total P (TP) were driven by freshwater
discharge at the sampling station 0 furthest upstream
(Figs. 5,6,7,8). Seasonal patterns were evident as
periods of elevated discharge and nutrient loads: (1) a
winter-spring period with elevated rainfall and runoff;
(2) a summer-fall period with maxima in years
experiencing TCs, contrasted with years without
summer-fall TCs (e.g., 1997) when elevated nutrient
and DOC loadings were not observed.
Some TCs grazed the coastline and had little effect
on loads (e.g., Gordon in 2000, Charley in 2004, Ana
in 2015), while storms that made landfall significantly
affected loads, e.g. Fran (1996), Floyd (1999),
Matthew (2016), Florence (2018). These differences
can be traced to three factors: (1) the storm track,
especially after landfall; (2) forward speed of the
storm; (3) amount of rainfall associated with the
storm; and (4) storm surges. Storms that remained
offshore or grazed the coastline (e.g. Gordon, Charley)
generally delivered little rainfall, with highest winds
and rainfall typically occurring to the right of the
storm and remaining offshore. Forward speed of TCs
strongly affected rainfall, especially once landfall
occurred. This was the case with Fran, Floyd,
Matthew, and Florence (Figs. 58); slow-moving,
high-rainfall events that appear to be increasing in
frequency (Paerl et al. 2019).
Freshwater discharge associated with TCs strongly
affected hydrologic characteristics of the NRE,
including water residence times. On average, the
flushing time of the NRE is about 2 months (Fig. 9),
and commonly exceeds 4 months during protracted
dry periods (e.g. 2007). Increased river discharge from
TCs with high precipitation, however, rapidly
increases the flushing rate of the estuary. Following
extreme floods associated with Matthew and Florence,
residence time of the NRE was only about 10 days,
and for Floyd less than 5 days.
Impacts of discharge from a high-volume flushing
event associated with Florence (Sept. 2018) are shown
as disruptions of vertical profiles of physical–chemical
properties (salinity, temperature, dissolved oxygen)
that also flushed phytoplankton biomass (as Chl-a)
from the system (Fig. 10). In contrast, events with
lower discharge (e.g. TC Ernesto in 2006) led to
elevated levels of DOC, TN and TP, with strong
vertical stratification and significant horizontal gradi-
ents of physical–chemical properties (Fig. 11). These
conditions of increased nutrient delivery favored algal
growth and formation of blooms as freshwater
discharge was not high enough to flush phytoplankton
from the estuary. Furthermore, freshwater discharge
was not sufficiently high to disrupt vertical density
123
Biogeochemistry (2020) 150:197–216 203
stratification, and these conditions supported a bloom
of the toxic dinoflagellate, Karlodinium veneficum
(Hall et al. 2008) (Fig. 11).
In the case of a tropical depression in July 2002 that
delivered substantial rainfall to coastal North Car-
olina, high discharge to the NRE and the nearby
Pamlico River flushed phytoplankton from the system
into the PS (Paerl et al. 2007). Nutrient-rich waters
then supported algal growth and blooms in the PS, a
much larger system than adjacent sub-estuaries with a
substantially longer residence time of up to one year
(Pietrafesa et al. 1996).
Significant differences in annual loadings of DOC
and nutrients occurred in years with and without TCs.
In years without TCs (1999, 2004, 2010), typical
seasonal patterns of DOC, TN and TP loadings were
observed (Figs. 5,6,7,8). In years with TCs
accompanied by moderate rainfall, up to half the
annual loadings of DOC and nutrients were associated
with storm events. In years with TCs accompanied by
very high rainfall, more than half the annual loadings
were associated with storm events. Given the sampling
protocol, we were not able to quantify additional
contributions from storm surges.
Summarizing, TCs with high rainfall have the
potential to double annual loadings of DOC and
nutrients to the NRE and PS. For TC Floyd (1999),
approximately 80% of annual N and 60% of the annual
P loads were attributed to surface runoff and subsur-
face groundwater (Paerl et al. 2001,2006). With
regard to organic matter, approximately 80% of annual
allochthonous POC and an equivalent percentage of
annual DOC inputs were attributable to floodwaters
from Floyd (Paerl et al., 2001,2006). For the Pamlico
Sound alone, this single event provided 60% of the
annual load (Bales 2003; Paerl et al. 2006).
Biogeochemical and ecological impacts
Hurricane Floyd struck eastern North Carolina in Sept.
1999, overwhelming the NRE with extremely high
freshwater discharge, and essentially turning it into a
‘pipeline’’ that emptied into the APS (Paerl et al.
2001,2006). This event led to very large discharge of
Fig. 5 Daily Neuse River freshwater discharge at the Fort Barnwell (USGS 02091814) gauging station upstream from the head of the
Neuse River Estuary, as shown in Fig. 4, for selected years
123
204 Biogeochemistry (2020) 150:197–216
freshwater overlying denser saline water, resulting in
strong, persistent vertical stratification, and extensive
hypoxia in bottom waters of the APS, with massive
fish and shellfish kills and an abrupt increase in fish
disease (Eby and Crowder 2002; Adams et al. 2003;
Paerl et al. 2006).
Prevailing hydrologic conditions in a given year
strongly affect overall impacts of TCs on estuarine and
coastal waters. For example, Hurricane Matthew in
2016 occurred during a ‘‘wet’’ year with above-
average discharge from winter through spring
(Fig. 12). Thus, impacts of Hurricane Matthew on
annual C, N and P loadings were masked by ‘‘high-
flow’’ conditions compared to TCs passing through the
NRE and its watershed during ‘‘dry’’ years (Paerl et al.
2018). Moreover, precipitation from Hurricane Mat-
thew was largely focused in the upper regions of the
watersheds, and the pulse of waters associated with
Matthew took 2–4 weeks to reach the NRE and
Pamlico Sound proper. Nutrient loadings following
Hurricane Matthew accounted for *50% of the
annual SRP loading and *20% of the annual DIN
load to the NRE and Pamlico Sound (Paerl et al. 2018).
In the first two weeks following Matthew, 25% of
annual C loading for 2016 was delivered to the estuary
(Osburn et al. 2019a,b). The majority (67%) of the C
load was DOC (Osburn et al. 2019a,b), similar to
observations for other TCs such as Floyd (Paerl et al.
2018).
Hurricane Florence stalled off the North Carolina
coast for several days from late September to early
October, 2018, and upon landfall delivered [70 cm
of rainfall to eastern NC and the NRE watershed (Paerl
et al. 2019). Similar to Floyd and Matthew, floodwa-
ters from Florence led to extensive freshening of the
NRE (Fig. 9). The sheer volume of freshwater
discharge and high flushing rates prevented salinity
stratification. Initial estimates of DOC loading suggest
that the concentration doubled near peak river dis-
charge, with Florence accounting for a 75% increase
of the annual DOC load to the NRE (cf. Fig. 8).
The combined effects of Hurricanes Floyd, Mat-
thew, and Florence on hydrologic, C, N and P loadings
to the NRE and APS systems in the past 20 years were
Fig. 6 Daily total nitrogen (TN) load at the head of the Neuse River Estuary
123
Biogeochemistry (2020) 150:197–216 205
unmatched in recorded history of hurricanes and TCs
for coastal North Carolina (Paerl et al. 2019). While
long-term C, N and P cycling dynamics of the legacy
loads delivered by these storms are still evolving,
short-term biogeochemical and trophic impacts are
evident. A notable example is expansion of the
hypoxic zone in the estuarine continuum following
Floyd that compressed finfish and shellfish habitats
(Eby and Crowder 2002; Eggleston et al. 2010).
Enhanced nutrient loads associated with TCs
(Figs. 58) stimulated phytoplankton production, but
effects varied in time and space, depending on
estuarine flushing rates and the magnitude of high-
nutrient freshwater discharge. For example, in condi-
tions of moderate discharge and nutrient enrichment
but freshwater discharge insufficiently high to exceed
phytoplankton growth rates and flush algae out of the
system, stimulation of phytoplankton biomass as Chl
awas evident in the NRE shortly after storm passage.
Examples of this response included TCs Isabel (2003),
Charley (2004), Ernesto (2006) and Joaquin (2015)
(Fig. 13). Conversely, a delayed phytoplankton
response to TCs with high rainfall and discharge,
was exemplified by Floyd (1999), Matthew (2016) and
Florence (2016) that essentially turned the NRE into a
‘pipeline’’ where phytoplankton growth was not
stimulated until months after the event (Fig. 13).
Under these conditions, a large proportion of the short-
term (days to weeks) growth response of phytoplank-
ton occurred in the larger, longer residence time
downstream Pamlico Sound (Paerl et al. 2007). The
NRE response can lag by a matter of weeks, depending
on how quickly high river flow recedes. Examples of
this scenario include Floyd (1999–2000) and Florence
(2018) (Fig. 13).
Some TCs such as Ernesto (2006) generated large
pulse loadings of nutrients in freshwater discharge,
producing optimal conditions for development of
Fig. 7 Daily total phosphorus (TP) load at the head of the Neuse River Estuary
123
206 Biogeochemistry (2020) 150:197–216
harmful algal blooms (HABs) of the toxic dinoflagel-
late, Karlodinium veneficum. These HABs occurred in
the mid-estuarine region of the microtidal NRE where
nutrient-rich freshwater discharge and moderate
flushing provided long enough water residence time
for blooms to proliferate (Hall et al. 2008) (Fig. 11).
Large phytoplankton blooms also occurred in the PS
with its longer residence time in response to nutrient
loadings in freshwater discharge following passage of
Hurricane Floyd (1999–2000) (Tester et al. 2003).
Freshening of coastal ecosystems in North Carolina
associated with an increased frequency of TCs and
associated precipitation affects salinity gradients in
the NRE-PS continuum, with periods of depressed
salinity extending well downstream (Paerl et al. 2006;
2018). These conditions favor low-salinity phyto-
plankton groups, such as chlorophytes and cyanobac-
teria (Pinckney et al. 1998; Hall et al. 2013; Paerl et al.
2013,2018). Other estuarine and coastal waters
experiencing increased discharge and flooding asso-
ciated with a higher frequency of major storm and
rainfall events show evidence of a similar
Fig. 8 Daily dissolved organic carbon (DOC) load based on concentrations measured at the head of the Neuse River Estuary
Fig. 9 Time series of flushing time of the Neuse River Estuary
in relation to the timing of ‘‘wet’’ tropical cyclones that resulted
in significant increases in river discharge. See Paerl et al. (2018)
for details on the objective definition of ‘‘wet’’ storms
123
Biogeochemistry (2020) 150:197–216 207
phytoplankton bloom response. For example in the
Mississippi Delta, northern Gulf of Mexico, increased
rainfall and flood events in the Mississippi watershed
produced large plumes of nutrient-rich freshwater that
extended into coastal bayous and bays (Bargu et al.
2019). These conditions promoted the downstream
expansion of harmful (toxic) cyanobacterial genera,
including Dolichospermum and Microcystis (Rieken-
berg et al. 2015; Bargu et al. 2019). In the APS, a
parallel scenario is observed in the brackish Albemarle
Sound that drains several rivers in eastern North
Carolina and southeastern Virginia, including the
Chowan and Roanoke. The Chowan River has a
history of harmful cyanobacterial blooms, or Cyano-
HABs (Dolichospermum and Microcystis) and is
currently experiencing a bloom resurgence (https://
www.albemarlercd.org/fighting-algal-blooms.html).
These systems have also experienced increased storm-
related freshwater and C, N and P loadings that create
periods of fresher and more nutrient rich conditions
that favors CyanoHAB expansion into oligohaline
Albemarle Sound where Dolichospermum,Microcys-
tis and Cylindrospermopsis populations have become
widespread and common (Calandrino and Paerl 2011;
NC DEQ 2019).
Increased DOC and DON loadings coincide with
increases of freshwater discharge and nutrient load-
ings associated with TCs. Bioassays conducted in-situ
on the New River Estuary, North Carolina showed that
organic matter in freshwater discharge stimulated
phytoplankton biomass and altered taxonomic com-
position, stimulating several dinoflagellate and
cyanobacterial taxa (Altman and Paerl 2012). These
findings suggest specific components of the DOM (i.e.,
DON) pool play a role in phytoplankton dynamics.
Bacterial production may also be stimulated by DOM
in freshwater discharge (allochthonous) or DOM
produced by phytoplankton (autochthonous) (Peierls
and Paerl 2010; Peierls and Paerl 2011).
Fig. 10 Physical–chemical impacts of freshwater discharge
resulting from Hurricane Florence (September, 2018) on the
Neuse River Estuary, NC. Shown are water column profiles
(dashed vertical lines show location of ModMon station profiles)
of salinity, temperature, dissolved oxygen, pH, chlorophyll a(as
an indicator of algal biomass) and turbidity, before (left hand
side) and after (right hand side) the storm made landfall
123
208 Biogeochemistry (2020) 150:197–216
Implications for carbon cycling
As observed for nutrient loadings, the increasing
intensity and frequency of TCs also affect C loading
and cycling in estuarine and coastal waters. Freshwa-
ter loads of nutrients and organic matter provide the
fuel for microbial consumption of oxygen, often
leading to extensive hypoxia and anoxia throughout
the APS (Buzzelli et al 2002; Paerl et al.
1998,2001,2006,2018) (Fig. 14). Furthermore,
breakdown and cycling of allochthonous organic
matter mediated by heterotrophic microbes (Peierls
and Paerl 2010) modulates nutrient availability, pri-
mary production of organic matter, and ultimately,
trophic state. The importance of ecosystem-scale DOC
loadings attributable to TCs are exemplified by
Hurricane Matthew (2016) which accounted for up
to 25% of the annual DOC load to the NRE and
Pamlico Sound (Osburn et al. 2019a,b), representing a
disproportionate impact on the annual DOC loading to
the estuarine system in 2016.
The source of this additional DOC loading was
largely a result of the flooding of freshwater wetlands
at the head of the estuary, shifting the quality of DOM
imported into the estuary from upstream, terrestrial-
sources to wetlands-derived sources following the
storm event (Rudolph et al. 2020; Osburn et al.
2019a,b; Table 2). Not only did this result in enhanced
DOC loading from the Neuse River to the NRE, but it
also enhanced DOC loading from the NRE to the
downstream Pamlico Sound, as the ‘‘pulse’’ of
wetland-derived DOC was ‘‘shunted’’ to the sound
(Rudolph et al. 2020; Osburn et al. 2019a,b; Houn-
shell et al. 2019; Table 2). In the weeks to months
following Hurricane Matthew, the wetland-derived
organic matter flushed into Pamlico Sound and was
oxidized to CO
2
thereby switching the system from a
CO
2
sink to a CO
2
source and changing the role of the
estuary in the processing of organic matter. (Osburn
et al. 2019a,b).
Changing quality and quantity of DOC flushed into
estuarine and coastal waters could have important
implications for the role of ecosystems, such as APS,
Fig. 11 A toxic dinoflagellate (Karlodinium veneficum) bloom associated with nutrient-enriched runoff from tropical storm Ernesto,
October, 2006, which set up strong vertical and horizontal salinity gradients in the NRE
123
Biogeochemistry (2020) 150:197–216 209
in the global C cycle (Bauer et al. 2013). With an
increase of extreme discharge events associated with
TCs, some estuaries, such as the Neuse River, may
switch from ‘processors’ of DOC to ‘pipelines’ with
direct export of terrestrial DOC to downstream sounds
and coastal waters, such as Pamlico Sound, which
themselves become important processors (Osburn
et al. 2019a,b; Hounshell et al. 2019). This could
result in estuaries and coastal waters experiencing
extended hypoxia and acidification (Wallace et al.
2014) as well as reorganizing coastal C cycles (Najjar
et al. 2018; Yan et al. 2020). Additional studies are
needed to assess the direct link between wetlands-
derived DOC flushed into estuarine and coastal waters
following TCs with observed CO
2
fluxes, but prelim-
inary results suggest these coastal ecosystems become
important locations for the transformation of this
wetland-derived DOC in the weeks and months
following storm events associated with extreme pre-
cipitation (Osburn et al. 2019a,b).
Fig. 12 River discharge, salinity and DOC for seven discrete discharge events in the Neuse River Estuary, starting with offshore storm
Joaquin September, 2015 and ending with Hurricane Matthew in September, 2016. From Hounshell et al. (2019)
123
210 Biogeochemistry (2020) 150:197–216
Additionally, following TCs with comparatively
less extreme precipitation, such as Hurricane Irene in
2014, Crosswell et al. (2014) observed a significant
release of CO
2
from the NRE and Pamlico Sound
following TC passage. Specifically, the authors
reported extensive DOM enrichment associated with
Hurricane Irene (2014) in the NRE and Pamlico
Sound, leading to a massive pulse of CO
2
-release to
the atmosphere, roughly equivalent to the annual
amount of CO
2
fixed by phytoplankton in these
systems (Crosswell et al. 2014). Results following
both Hurricane Matthew, a disproportionally high
precipitation event, as well as following Hurricane
Irene, demonstrate the importance of TCs on control-
ling riverine DOM loading and processing under a
range of TC characteristics.
DOM quality of exported DOC storm loads is also
likely an important factor in the response of estuaries
to TCs. For example, Other studies have reported
similar changes of DOM quantity and quality follow-
ing hurricanes. Letourneau and Medeiros (2019)
observed increases of DOC concentrations of terres-
trial quality following passage of Hurricane Matthew,
despite little change in freshwater discharge to Geor-
gia estuaries. The increasing terrestrial quality of
DOM associated with freshwater discharge was linked
to increased microbial degradation (Letourneau and
Medeiros 2019), pointing to potential linkages of TCs
to DOM quality, microbial degradation, and CO
2
production. Lu and Liu (2019) observed significant
enrichment of DOM in four Texas rivers draining into
the northern Gulf of Mexico following major storms.
The authors noted that DOM quality shifted from
protein-like and lipid-like compounds at base flow
conditions, to lignin, tannin and condensed aromatic
structure during high freshwater discharge. Similarly,
in the Newport River Estuary, near the APS, increases
in aromatic DOC were correlated to higher microbial
mineralization rates of aromatic C (Osburn et al.
2019b). Thus, terrestrial DOM flushed into estuarine
systems during high-flow conditions has been traced to
mobilization of organic matter from the watersheds
and wetlands due to flooding, consistent with findings
in the NRE and Pamlico Sound (Rudolph et al. 2020).
Results of previous studies and evidence presented
here show that increased TCs exert a disproportionate
impact on C, N and P loadings to estuarine and coastal
waters, with qualitative and quantitative effects on
primary producers and associated microheterotrophs
(Paerl et al. 2006,2018; Peierls et al. 2003,2011).
Fig. 13 Discharge (m
3
s
-1
) in relation to phytoplankton production (as Chl a) downstream in the Neuse River Estuary-Pamlico Sound
estuarine continuum
123
Biogeochemistry (2020) 150:197–216 211
Short- and long-term biogeochemical impacts, includ-
ing coastal C, N and P cycling, oxygen dynamics,
habitat alteration, and trophodynamics deserve careful
scrutiny as we have entered a ‘‘new normal’’ with
increased TCs and associated extremes of precipita-
tion and freshwater discharge (Seneviratne et al. 2012;
Wetz and Yoskowitz 2013; Asadieh and Krakauer
2015; Paerl et al. 2019).
Fig. 14 Conceptual figure, showing the interactive effects of
TC-related freshwater discharge, DOC and nutrient loading and
wind mixing on physical structure of the water column,
phytoplankton and associated microbial activities and biogeo-
chemical responses, including hypoxia and air–water CO
2
exchange in a lagoonal estuary like the Neuse River Estuary.
Illustrated are the before, during and after TC scenarios. During
moderate storms, the DOC and DON from the storms lead to a
down estuary bloom. During severe storms, the DOC and DON
from the storms is flushed out of the estuary into Pamlico Sound
123
212 Biogeochemistry (2020) 150:197–216
Acknowledgements We appreciate the assistance of J.
Braddy, A. Joyner, H. Walker, B. Abare, R. Sloup and all
students and technicians that participated in the field and
laboratory work supporting this publication. This research was
funded by NSF Projects DEB 1119704, DEB 1240851, OCE
0825466, OCE 0812913, OCE 1705972, OCE 1706009, and
CBET 0932632, North Carolina Department of Environmental
Quality (ModMon Program), Lower Neuse Basin Association,
North Carolina Sea Grant Program, and the University of North
Carolina Water Resources Research Institute.
References
Adams SM, Greeley MS, Law JM, Noga EJ, Zelikoff JT (2003)
Application of multiple sublethal stress indicators to assess
the health of fish in Pamlico Sound following extensive
flooding. Estuaries 26:1365–1382
Alber M, Sheldon JE (1999) Use of a date-specific method to
examine variability in the flushing times of Georgia estu-
aries. Estuar Coastal Shelf Sci 49:469–482
Allan RP, Soden BJ (2008) Atmospheric warming and the
amplification of precipitation extremes. Science
321:1481–1484
Altman JC, Paerl HW (2012) Composition of inorganic and
organic nutrient sources influences phytoplankton com-
munity structure in the New River Estuary, North Carolina.
Aquat Ecol 42:269–282
Arar EJ, Budde WL, Behymer TD (1997) Methods for the
Determination of Chemical Substances in Marine and
Environmental Matrices. EPA/600/R-97/072. National
Exposure Research Laboratory, U.S. Environmental Pro-
tection Agency, Cincinnati, OH.
Asadieh B, Krakauer NY (2015) Global trends in extreme pre-
cipitation: climate models versus observations. Hydrol
Earth Syst Sci 19:877–891
Bales JD (2003) Effects of hurricane floyd inland flooding,
September–October 1999, on tributaries to Pamlico Sound,
North Carolina. Estuaries 26:1319–1328
Bales JD, Oblinger CJ, Sallenger AH (2000) Two months of
flooding in eastern North Carolina, September–October
1999: hydrologic, water-quality, and geologic effects of
Hurricanes Dennis, Floyd, and Irene. U.S. Geological
Survey Water-Resources Investigations Report 00-4093.
Bargu S, Justic D, White J, Lane R, Day J, Paerl H, Raynie R
(2019) Mississippi River diversions and phytoplankton
dynamics in deltaic Gulf of Mexico estuaries: a review.
Estuar Coast Shelf Sci 221:39–52
Bianchi TS, Garcia-Tigreros F, Yvon-Lewis SA, Shields M,
Mills HJ, Butman D, Walker N (2013) Enhanced transfer
of terrestrially derived carbon to the atmosphere in a
flooding event. Geophys Res Lett 40:116–122
Bowen JD, Hieronymus J (2000 ) Neuse River Estuary modeling
and monitoring project stage 1: predictions and uncertainty
analysis of response to nutrient loading using a mechanistic
eutrophication model. University of North Carolina North
Carolina Water Resources Research Institute report 325-D.
Boyer JN, Christian RR, Stanley DW (1993) Patterns of phy-
toplankton primary productivity in the Neuse River estu-
ary, North Carolina, USA. Mar Ecol Progr Ser 97:287–297
Boyer JN, Stanley DW, Christian RR (1994) Dynamics of NH
4
?
and NO
3
-
uptake in the water column of the Neuse River
estuary, North Carolina. Estuaries 17:361–371
Buzzelli CP, Luettich RA, Powers SP, Peterson CH, McNinch
JE, Pinckney JL, Paerl HW (2002) Estimating the spatial
extent of bottom-water hypoxia and habitat degradation in
a shallow estuary. Mar Ecol Progr Ser 230:103–112
Calandrino E, Paerl HW (2011) Determining the potential for
the proliferation of the harmful cyanobacterium Cylin-
drospermopsis raciborskii in Currituck Sound, North
Carolina. Harmful Algae 11:1–9
Christian RR, Boyer JN, Stanley DW (1991) Multi-year distri-
bution patterns of nutrients within the Neuse River Estuary,
North Carolina. Mar Ecol Progr Ser 71:259–274
Table 2 DOC mass loading from Neuse River and freshwater wetlands into the NRE-PS, in response to Hurricane Matthew
Location Total DOC mass (Gg C) NRE DOC (%) PS DOC (%)
Fort Barnwell, NC
1d
a
0.436 9.2 3.1
7d
a
3.042 64.1 22.0
Wetlands
Max
b
2.260 47.7 16.3
Mean
c
0.965 20.4 7.0
NRE
Max
d
4.741 – 34.2
PS
Max
e
13.849 – –
Mean [DOC] value from high discharge (7.429 mg C L
-1
). Maximum [DOC] from freshwater wetlands in autumn (14.4 mg C L
-1
).
Mean [DOC] from freshwater wetlands in autumn (6.15 mg C L
-1
). Maximum [DOC] stock change from NRE. Maximum [DOC]
stock change from PS. From Rudolph et al. 2020
123
Biogeochemistry (2020) 150:197–216 213
Crosswell JR, Wetz MS, Hales B, Paerl HW (2014) Extensive
CO
2
emissions from shallow coastal waters during passage
of Hurricane Irene (August 2011) over the Mid-Atlantic
Coast of the U.S.A. Limnol Oceanogr 59:1651–1665
Eby LA, Crowder LB (2002) Hypoxia-based habitat compres-
sion in the Neuse River Estuary: context dependent shifts in
behavioral avoidance thresholds. Can J Fish Aquat Sci
59:952–965
Eggleston DB, Reyns NB, Etherington LL, Plaia G, Xie L
(2010) Tropical storm and environmental forcing on
regional blue crab settlement. Fish Oceanogr 19(2):89–106
Frankson R, Kunkel K, Stevens L, Easterling D, Boyles R,
Wootten A, Aldridge H, Sweet W (2019) State Climate
Summaries 149-NC May 2019 Revision. NOAA National
Centers for Environmental Information. https://
statesummaries.ncics.org/downloads/NC-screen-hi.pdf
Fulton RS, Paerl HW (1988) Effects of the blue-green alga
Microcystis aeruginosa on zooplankton competitive rela-
tions. Oecologia 76(3):383–389
Hall NS, Litaker RW, Fensin E, Adolf JE, Place AR, Paerl HW
(2008) Environmental factors contributing to the devel-
opment and demise of a toxic dinoflagellate (Karlodinium
veneficum) bloom in a shallow, eutrophic, lagoonal estuary.
Estuar Coasts 31:402–418
Hall NS, Paerl HW, Peierls BL, Whipple AC, Rossignol KL
(2013) Effects of climatic variability on phytoplankton
biomass and community structure in the eutrophic,
microtidal, New River Estuary, North Carolina, USA.
Estuar Coast Shelf Sci 117:70–82
Hirsch RM, De Cicco L (2015) User guide to Exploration and
Graphics for RivEr Trends (EGRET) and data Retrieval: R
packages for hydrologic data. Tech. Rep. Techniques and
Methods book 4, ch. A10, US Geological Survey, Reston,
Virginia. http://pubs.usgs.gov/tm/04/a10/
Hirsch RM, Moyer DL, Archfield SA (2010) Weighted regres-
sions on time, discharge, and season (WRTDS), with an
application to Chesapeake Bay river inputs. J Am Water
Res Assoc 46:857–880
Holland GJ, Webster PJ (2007) Heightened tropical cyclone
activity in the North Atlantic: natural variability of climate
trend? Phil Trans R Soc A. https://doi.org/10.1098/rsta.
2007.2083
Hopkinson CS, Vallino JJ (1995) The relationships among
man’s activities in watersheds and estuaries: a model of
runoff effects on patterns of estuarine community meta-
bolism. Estuaries 18:598–621
Hounshell AG, Rudolph JC, Van Dam BR, Hall NS, Osburn CL,
Paerl HW (2019) Extreme weather events modulate pro-
cessing and export of dissolved organic carbon in the
Neuse River Estuary, NC. Estuar Coast Shelf Sci
219:189–200. https://doi.org/10.1016/j.ecss.2019.01.020
Kennish M, Paerl HW (2010) Coastal lagoons: critical habitats
of environmental change. CRC Marine Science Series.
CRC Press, Boca Raton, FL
Konrad CE, Perry LB (2010) Relationships between tropical
cyclones and heavy rainfall in the Carolina region of the
USA. Internat J Climatol: Royal Met Soc 30:522–534
LANDSAT 8. NASA Earth Science Disasters Program. https://
disasters.nasa.gov/hurricane-florence-2018/nasa-landsat-
8-captures-debris-imagery-hurricane-florence
Lehmann J, Coumou D, Frieler K (2015) Increased record-
breaking precipitation events under global warming. Clim
Change 132:501–515
Letourneau ML, Medeiros PM (2019) Dissolved organic matter
composition in a marsh-dominated estuary: response to
seasonal forcing and to the passage of a hurricane. J Geo-
phys Res: Biogeosci 124(6):1545–1559
Lu K, Liu Z (2019) Molecular level analysis reveals changes in
chemical composition of dissolved organic matter from
South Texas Rivers after high flow events. Front Mar Sci.
https://doi.org/10.3389/fmars.2019.00673
Luettich RA, McNinch JE, Paerl HW, Peterson CH, Wells JT,
Alperin MA, Martens CS, Pinckney JL (2000) Neuse River
Estuary modeling and monitoring project stage 1:
hydrography and circulation, water column nutrients and
productivity, sedimentary processes and benthic-pelagic
coupling, and benthic ecology. North Carolina Water
Resources Research Institute report 325 B.
Lung WS, Paerl HW (1988) Modeling blue-green algal blooms
in the lower Neuse River. Wat Res 22(7):895–905
Mallin MA, Corbett CA (2006) How hurricane attributes
determine the extent of environmental effects: multiple
hurricanes and different coastal systems. Estuar Coasts
29(6):1046–1061
McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB,
Groffman PM, McDowell WH (2003) Biogeochemical hot
spots and hot moments at the interface of terrestrial and
aquatic ecosystems. Ecosystems 6(4):301–312
Najjar RG, Herrmann M, Alexander R, Boyer EW, Burdige DJ,
Butman D, Feagin RA (2018) Carbon budget of tidal
wetlands, estuaries, and shelf waters of Eastern North
America. Glob Biogeochem Cycl 32(3):389–416
Neuse River Estuary Modeling and Monitoring Program for the
Neuse River Estuary, ModMon, http://paerllab.web.unc.
edu/projects/modmon/. Univ. of North Carolina at Chapel
Hill, Institute of Marine Sciences, Morehead City, NC
(2020).
NOAA Hurricane Center (2019): http://www.nhc.noaa.gov as
plotted from Our World in Data https://ourworldindata.org/
grapher/frequency-north-atlantic-hurricanes.
North Carolina Department of Environment and Natural
Resources, Division of Water Quality (2001) Phase II of
the total maximum daily load for total nitrogen to the
Neuse River Estuary, North Carolina. December 2001.
North Carolina Department of Environmental Quality (2019)
Algal Blooms. https://deq.nc.gov/about/divisions/water-
resources/water-resources-data/water-sciences-home-
page/ecosystems-branch/algal-blooms
Osburn CL, Rudolph JC, Paerl HW, Hounshell AG, Van Dam
BR (2019a) Lingering carbon cycle effects of Hurricane
Matthew in North Carolina’s coastal waters. J Geophys
Res. https://doi.org/10.1029/2019GL082014
Osburn CL, Atar JN, Boyd TJ, Montgomery MT (2019b)
Antecedent precipitation influences the bacterial process-
ing of terrestrial dissolved organic matter in a North Car-
olina estuary. Estuar Coast Shelf Sci 221:119–131
Paerl HW (1983) Factors regulating nuisance blue-green algal
bloom potentials in the lower Neuse River, North Carolina.
UNC Water Resources Research Institute Report Report
No. 188. Water Resources Research Institute of the
University of North Carolina, Raleigh, NC.
123
214 Biogeochemistry (2020) 150:197–216
Paerl HW (2005 ) Ecological effects of a recent rise in Atlantic
hurricane activity on North Carolina’s Pamlico sound
system: putting hurricane Isabel in perspective. In: Sellner
KG (ed) Hurricane Isabel in perspective. Chesapeake
research Consortium, CRC Publications 05-160, Edgewa-
ter, MD, pp 3–18.
Paerl HW, Mallin MA, Donahue CA, Go M, Peierls BL (1995)
Nitrogen loading sources and eutrophication of the Neuse
River estuary, NC: Direct and indirect roles of atmospheric
deposition. UNC Water Resources Research Institute
Report No. 291. Water Resources Research Institute of the
University of North Carolina, Raleigh, NC.
Paerl HW, Pinckney JL, Fear JM, Peierls BL (1998) Ecosystem
responses to internal and watershed organic matter loading:
consequences for hypoxia in the eutrophying Neuse River
Estuary, North Carolina, USA. Mar Ecol Progr Ser
166:17–25
Paerl HW, Bales JD, Ausley LW, Buzzelli CP, Crowder LB,
Eby LA, Fear JM, Go M, Peierls BL, Richardson TL,
Ramus JS (2001) Ecosystem impacts of 3 sequential hur-
ricanes (Dennis, Floyd and Irene) on the US’s largest
lagoonal estuary, Pamlico Sound. NC Proc Natl Acad Sci
USA 98(10):5655–5660
Paerl HW, Valdes LM, Joyner AR, Peierls BL, Buzzelli CP,
Piehler MF, Riggs SR, Christian RR, Ramus JS, Clesceri
EJ, Eby LA, Crowder LW, Luettich RA (2006) Ecological
response to hurricane events in the Pamlico Sound System,
NC and implications for assessment and management in a
regime of increased frequency. Estuar Coasts
29:1033–1045
Paerl HW, Valdes LM, Joyner AR, Winkelmann V (2007)
Phytoplankton indicators of ecological change in the
nutrient and climatically-impacted Neuse River-pamlico
sound system. North Carolina Ecol Appl 17(5):88–101
Paerl HW, Rossignol KL, Guajardo R, Hall NS, Joyner AR,
Peierls BL, Ramus JS (2009) FerryMon: Ferry-based
monitoring and assessment of human and climatically
driven environmental change in the Albemarle-Pamlico
Sound system. Environ Sci Technol 43:7609–7613
Paerl HW, Rossignol KL, Hall NS, Peierls BL, Wetz MS (2010)
Phytoplankton community indicators of short- and long-
term ecological change in the anthropogenically and cli-
matically impacted Neuse River Estuary, North Carolina,
USA. Estuar Coasts 33:485–497
Paerl HW, Hall NS, Peierls BL, Rossignol KL, Joyner AR
(2013) Hydrologic variability and its control of phyto-
plankton community structure and function in two shallow,
coastal, lagoonal ecosystems: the Neuse and New River
Estuaries, North Carolina, USA. Estuaries Coasts
37(Suppl. 1):31–45. https://doi.org/10.1007/s12237-013-
9686-0
Paerl HW, Crosswell JR, Van Dam B, Hall NS, Rossignol KL,
Osburn CL, Hounshell AG, Sloup RS, Harding LW Jr
(2018) Two decades of tropical cyclone impacts on North
Carolina’s estuarine carbon, nutrient and phytoplankton
dynamics: implications for biogeochemical cycling and
water quality in a stormier world. Biogeochemistry. https://
doi.org/10.1007/s10533-018-0438-x
Paerl HW, Hall NS, Hounshell AG, Luettich RA, Rossignol KL,
Osburn CL, Bales J (2019) Recent increase in catastrophic
tropical cyclone flooding in coastal North Carolina, USA:
long-term observations suggest a regime shift. Sci Rep
9(1):1–9
Peierls BL, Christian RR, Paerl HW (2003) Water quality and
phytoplankton as indicators of hurricane impacts on a large
estuarine ecosystem. Estuaries 26:1329–1343
Peierls BL, Paerl HW (2010) Temperature, organic matter, and
the control of bacterioplankton in the Neuse River and
Pamlico Sound estuarine system. Aquat Microb Ecol
60:139–149
Peierls BL, Paerl HW (2011) Longitudinal and depth variation
of bacterioplankton productivity and related factors in a
temperate estuary. Estuar Coast Shelf Sc 95(1):207–215
Peierls BL, Hall NS, Paerl HW (2012) Non-monotonic
responses of phytoplankton biomass accumulation to
hydrologic variability: a comparison of two coastal plain
North Carolina estuaries. Estuar Coasts 35:1376–1392
Pietrafesa LJ, Janowitz GS, Chao T-Y, Weisberg TH, Askari F,
Noble E (1996) The physical oceanography of pamlico
sound. UNC Sea Grant Publication UNC-WP-86-5
Pinckney JL, Paerl HW, Harrington MB, Howe KE (1998)
Annual cycles of phytoplankton community-structure and
bloom dynamics in the Neuse River Estuary North Car-
olina. Mar Biol 131:371–381
Pinckney JL, Millie DF, Vinyard BT, Paerl HW (1997) Envi-
ronmental controls of phytoplankton bloom dynamics in
the Neuse River Estuary, North Carolina, USA. Can J Fish
Aquat Sci 54(11):2491–2501
Riekenberg J, Bargu S, Twilley R (2015) Phytoplankton com-
munity shifts and harmful algae presence in a diversion
influenced estuary. Estuar Coasts 38:2213–2226
Rudek J, Paerl HW, Mallin MA, Bates PW (1991) Seasonal and
hydrological control of phytoplankton nutrient limitation
in the lower Neuse River Estuary, North Carolina. Mar
Ecol Progr Ser 75:133–142
Rudolph JC, Arendt CA, Hounshell AG, Paerl HW, Osburn CL
(2020) Use of geospatial, hydrologic, and geochemical
modeling to determine the influence of wetland-derived
organic matter in coastal waters in response to extreme
weather events. Front Mar Sci. https://doi.org/10.3389/
fmars.2020.00018
Seneviratne SI, Nicholls N, Easterling D, Goodess CM and
others (2012) Ch. 3: Changes in climate extremes and their
impacts on the natural physical environment. In: Field CD,
Barros V, Stocker TF, Dahe Q, et al. (Eds) Managing the
risks of extreme events and disasters to advance climate
change adaptation. A special report of Working Groups I
and II of the Intergovernmental Panel on Climate Change
(IPCC). Cambridge University Press, Cambridge,
109–230.
Stow CA, Borsuk ME, Stanley DW (2001) Long-term changes
in watershed nutrient inputs and riverine exports in the
Neuse River, North Carolina. Water Res 35:1489–1499
Tester PA, Varnam SM, Culver ME, Eslinger DL et al (2003)
Airborne detection of ecosystem responses to an extreme
event: phytoplankton displacement and abundance after
hurricane induced flooding in the Albemarle-Pamlico
Sound system. Estuaries 26:1353–1364
Valdes-Weaver LM, Piehler MF, Pinckney JL, Howe KE,
Rosignol KL, Paerl HW (2006) Long-term temporal and
spatial trends in phytoplankton biomass and class-level
taxonomic composition in the hydrologically variable
123
Biogeochemistry (2020) 150:197–216 215
Neuse-Pamlico estuarine continuum, NC, USA. Limnol
Oceanogr 51(3):1410–1420
Wallace RB, Baumann H, Grear JS, Aller RC, Gobler CJ (2014)
Coastal ocean acidification: the other eutrophication
problem. Estuar Coastal Shelf Sci 148:1–13
Webster PJ, Holland GJ, Curry JA, Chang HR (2005) Changes
in tropical cyclone number, duration, and intensity in a
warming environment. Science 309:1844–1846
Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a
in the presence of chlorophyll b and pheopigments. Limnol
Oceanogr 39:1985–1992
Wetz MS, Yoskowitz DW (2013) An ‘‘extreme’’ future for
estuaries? Effects of extreme climatic events on estuarine
water quality and ecology. Mar Pollut Bull 69:7–18.
https://doi.org/10.1016/j.marpolbul.2013.01.020
Wuebbles D, Meehl G, Hayhoe K et al (2014) CMIP5 climate
model analyses: climate extremes in the United States. Bull
Am Meteorol Soc 95:571–583. https://doi.org/10.1175/
BAMS-D-12-00172.1
Yan G, Labonte JM, Quigg A, Kaiser K (2020) Hurricanes
accelerate dissolved organic carbon cycling in coastal
ecosystems. Front Marine Sci. https://doi.org/10.3389/
fmars.2020.00248
Publisher’s Note Springer Nature remains neutral with
regard to jurisdictional claims in published maps and
institutional affiliations.
123
216 Biogeochemistry (2020) 150:197–216
... To date the impacts of TCs on phytoplankton ecology have been reported from relatively few locations and events (e.g. Tsuchiya et al., 2014;Anglès et al., 2015;Paerl et al., 2018Paerl et al., , 2020. ...
... With >70% of the world's population residing in coastal watersheds (Vitousek et al., 1997;Vörösmarty et al., 2000), most estuaries are already under pressure from poor water quality (Boesch et al., 2001;Paerl et al., 2006), which is exacerbated by the effects of climate variability and change (Trenberth, 2011;Seneviratne et al., 2012;IPCC, 2013;Paerl et al., 2018Paerl et al., , 2020. Large watersheds discharging to estuaries can act as concentrating mechanisms for the high precipitation load associated with many TCs. ...
... Large watersheds discharging to estuaries can act as concentrating mechanisms for the high precipitation load associated with many TCs. Therefore, advection combined with significant inputs of suspended and dissolved matter, nutrients, increased turbidity and reduced salinity are of greater significance nearshore relative to the open ocean (Paerl et al., 2018(Paerl et al., , 2020Osburn et al., 2019;Yan et al., 2020;Asmala et al., 2021). On the time-scale of days to weeks the impacts of a TC on phytoplankton ecology are likely to be dominated by the amount of rainfall and the residence time of the receiving water body (Paerl et al., 2018). ...
Article
Full-text available
Following the passage of a tropical cyclone (TC) the changes in temperature, salinity, nutrient concentration, water clarity, pigments and phytoplankton taxa were assessed at 42 stations from eight sites ranging from the open ocean, through the coastal zone and into estuaries. The impacts of the TC were estimated relative to the long-term average (LTA) conditions as well as before and after the TC. Over all sites the most consistent environmental impacts associated with TCs were an average 41% increase in turbidity, a 13% decline in salinity and a 2% decline in temperature relative to the LTA. In the open ocean, the nutrient concentrations, cyanobacteria and picoeukaryote abundances increased at depths between 100 and 150 m for up to 3 months following a TC. While at the riverine end of coastal estuaries, the predominate short-term response was a strong decline in salinity and phytoplankton suggesting these impacts were initially dominated by advection. The more intermediate coastal water-bodies generally experienced declines in salinity, significant reductions in water clarity, plus significant increases in nutrient concentrations and phytoplankton abundance. These intermediate waters typically developed dinoflagellate, diatom or cryptophyte blooms that elevated phytoplankton biomass for 1–3 months following a TC.
... Strong vertical mixing, as well as upwelling and oceanic eddies, caused by typhoons will supply nutrients to the surface layer from the bottom in the open sea (Fogel et al., 1999;Shibano et al., 2011;Guan et al., 2021). In nearshore areas, riverine discharge plays an important role in the nutrient enrichment of seawater by delivering nutrients from land (Zhao et al., 2009;Qiu et al., 2019;Baek et al., 2020;Paerl et al., 2020a). Given that phytoplankton growth is strongly influenced by temperature, salinity, and nutrient concentration, it is not surprising that these typhoon events can result in changes to the phytoplankton community and biomass, thereby influencing HAB occurrence or development (Shibano et al., 2011;Chung et al., 2012;Aoki et al., 2019). ...
... Consequently, the biophysical responses of the upper ocean to typhoon passage have been widely studied using satellite observations and numerical simulations in numerous cases (e.g., Shibano et al., 2011;Liu et al., 2020). However, suspended sediments, chromophore-containing dissolved organic matter, and reflections from ocean bottom will impose strong interference in achieving reliable chlorophyll values from remote-sensing techniques in the nearshore areas, especially estuaries (Osburn et al., 2019;Paerl et al., 2020a;Asmala et al., 2021). Furthermore, the temporal and spatial dynamics of phytoplankton assemblage and community cannot be easily described by remote sensing of Chl a. ...
... Previous studies suggest that river discharge from the areas of typhoon-induced floods contributes abundant terrestrial nutrients to estuarine and coastal waters (Chung et al., 2012;Chen et al., 2018;Paerl et al., 2020a;Asmala et al., 2021). The negative relationship between salinity and DIN, as well as DSi, showed that they were related to freshwater input. ...
Article
Full-text available
Extensive multi-species harmful algal blooms (HABs) were triggered by Super Typhoon Lekima in Laizhou Bay (Bohai Sea) in August 2019. After conducting two field cruises before and after the typhoon passage, we employed both high-performance liquid chromatography (HPLC)-pigment and microscopic methods to study the changes in the phytoplankton community and biomass. Following the passage of Lekima, the average surface salinity decreased, while dissolved inorganic nitrogen and dissolved silicate concentrations increased in the study area. The phytoplankton abundance and Chl a significantly increased after the typhoon event. Post-typhoon, the highest abundance values of Pseudo-nitzschia spp., Noctiluca scintillans, and Coscinodiscus spp. reached 10 6 cells/L and those of Bacillaria paxillifera, Ceratium spp., and Gymnodinium catenatum were in the order of 10 5 cells/L. HPLC-pigment CHEMTAX analysis showed that the biomass (Chl a) of dinoflagellates, diatoms, cryptophytes, chlorophytes, and haptophytes increased significantly after the typhoon. The increase in Chl a concentration was mainly attributable to large-sized phytoplankton, which are mostly diatoms and dinoflagellates. This study highlights that typhoons may cause HABs by introducing large amounts of freshwater and nutrients and change the phytoplankton community in a temperate and inner bay.
... The damming effects on nitrogen dynamics are influenced by climatic conditions, particularly by extreme climate events (e.g., rainstorms and droughts). For example, rainstorms can increase sluicing to produce nutrient pluses and promote nitrogen transportation downstream (Chen et al., 2012;Aguilera and Melack, 2018;Kleinteich et al., 2020;Paerl et al., 2020;Yi et al., 2020). Drought events can enhance the damming impacts on water cycles (Jiang et al., 2021a) and subsequently modify nitrogen biogeochemical cycles (Bruesewitz et al., 2017;Douglas et al., 2021). ...
... In any case, however, nitrogen pollutants will still be transported by rainstorms to the lower reaches and river estuary after dry periods. Previous studies reported that the nitrogen concentrations could increase by several times or even dozens of times during a storm event (Chen et al., 2012;Kleinteich et al., 2020), and storm-induced nitrogen load could contribute 50-80% annual nitrogen flux (Paerl et al., 2020). The resulting pulsed biogeochemical signals (Aguilera and Melack, 2018;Yi et al., 2020;Kleinteich et al., 2020) would cause a huge impact on the estuarine ecosystem. ...
Article
Damming and drought have dramatically altered water cycle dynamics in rivers, which further affects nitrogen biogeochemical cycles; however, their combined effects have rarely been studied, especially for ephemeral rivers with variable water flows. Taking the Dagu River of North China as the study area, we examined the spatiotemporal variability of nitrogen in river water and its relation to damming and drought. The total nitrogen (TN), dissolved inorganic nitrogen (DIN) and NO3¯ concentrations varied significantly in space and time, but the NH4⁺ and NO2¯ concentrations changed little. Spatially, compared with the upper reaches, the TN, DIN and NO3¯ concentrations in the lower reaches decreased by 71%, 81% and 85%, respectively, which was concurrent with the isotopic enrichment of nitrate. Temporally, their concentrations in dry seasons were more than twice of wet seasons, and increased from 2018 (normal year) to 2019 (dry year). The cascade dams may promote the NO3¯ removal towards the lower reaches through assimilation, which combined with nitrification and strong evaporation to enhance δ¹⁸O–NO3¯ enrichment and disproportionate δ¹⁵N–NO3¯/δ¹⁸O–NO3¯ ratio. Further, the damming effects can be aggravated by droughts because of no flow, extended nitrogen residence time and increased groundwater discharge with higher nitrogen contents, which jointly elevated the nitrogen level. Hence, the combined effects of damming and drought should be fully considered for management of water environment and resources in regions with ephemeral rivers.
... • There is a clear relationship between SST and the number of tropical events, although the correlation is much more significant if it is made with higher category hurricanes (MH) (Elsner et al., 2008). • In relation to the above, an increase in floods has been detected due to the aforementioned increase in higher category cyclones (Paerl et al., 2020), which is consistent with an increase in precipitation per event (IPCC, 2021). • As the path of tropical cyclones slows down their damage capacity increases, in terms of total precipitation (Gori et al., 2022), since it has been shown that this is inversely proportional to the speed of movement (Kossin, 2018). ...
Article
Full-text available
This study analyzes tropical disturbances in a region usually not affected by these events, the southeastern North Atlantic. This is an extensive area between Macaronesia and the coasts of northwest Africa and the southwest of the Iberian Peninsula. In the context of climate change, a statistical analysis has been conducted of the main database of the National Hurricane Center for the Atlantic basin, as well as a bibliographical compilation, in order to analyze the temporal and spatial evolution of these phenomena. The starting hypothesis is to verify the existence of an increase in the risk of these situations in the region of study, through research that characterizes and charts these phenomena. The results indicate that, although with long periods of recurrence, some events with notable impacts had occurred before the first systematic records were kept. In addition, over the last fifty years, a much more reliable period from a scientific perspective, there has been an increase in their number, especially in recent decades. Furthermore, an approximate estimate is made of the population likely to be affected by tropical disturbances, which estimates that more than twenty million people are at risk.
... The coastal North Carolina region in particular faces increased risk of storm-induced microbial community disruption due to long residence times (~1 year) characterizing the local Albemarle-Pamlico estuarine system that flows into coastal North Carolina marine waters (Paerl et al., 2001). This region has seen doubling of annual nitrogen loads, tripling of annual phosphorus loads, and enough organic carbon input to change the coastal region from a net sink to a net source of CO 2 during years with at least one major storm (~10 6 kg N, ~10 5 kg P, and ~ 10 7 kg DOC input over a 2-week period following Florence in 2018; Paerl et al., 2018Paerl et al., , 2020. Hurricane Matthew in 2016 significantly impacted the local ecosystem, accounting for ~25% of the total annual carbon input to the Neuse-Pamlico Estuary . ...
Article
Full-text available
Hurricane frequencies and intensities are expected to increase under warming climate scenarios, increasing potential to disrupt microbial communities from steady-state conditions and alter ecosystem function. This study shows the impact of hurricane season on microbial community dynamics within the barrier island system of Outer Banks, North Carolina. We found that the passage of two sequential energetic hurricanes in 2018 (Florence and Michael) were correlated with shifts in total and active (DNA and RNA) portions of bacterial communities but not in archaeal communities, and within surface waters but not within the sediment. These microbial community shifts were distinct from non-hurricane season conditions, suggesting significant implications for nutrient cycling in nearshore and offshore environments. Hurricane-influenced marine sites in the coastal North Atlantic region had lower microbial community evenness and Shannon diversity, in addition to increased relative abundance of copiotrophic microbes compared to non-hurricane conditions. The abundance of functional genes associated with carbon and nitrogen cycling pathways were also correlated with the storm season, potentially shifting microbial communities at offshore sites from autotroph-dominated to heterotroph-dominated and leading to impacts on local carbon budgets. Understanding the geographic- and system-dependent responses of coastal microbial communities to extreme storm disturbances is critical for predicting impacts to nutrient cycling and ecosystem stability in current and future climate scenarios.
... In many mountainous regions, rainfall/runoff is considered to be the main cause triggering landslides/slope failures. With the intensification of global and regional climate change, extreme rainfall events and huge flooding have occurred frequently in recent years (Paerl et al. 2020;Wei et al. 2020). The decrease in matric suction in the unsaturated zone caused by rainwater infiltration under torrential rain is considered the main cause of the landslide/slope failure initiation (Zhu et al. 2020). ...
Article
Full-text available
Limited by the independence and its defects of each general software package, simultaneous analysis of runoff, seepage, and large-deformation analysis is still an inevitable challenge. Generally, one of seepage, landslide-related large-deformation, and runoff is ignored or indirectly assessed during unsaturated soil landslide runout simulation. To provide a brand new solution, this paper declares a local shear strength (LSS) method to evaluate rainfall/runoff-induced reduction of the unsaturated soil shear strength. After that, a hybrid coupled hydro-mechanical framework is proposed to simulate rainfall/runoff-induced landslide runout within an unsaturated soil slope. The decrease in local shear strength corresponding to the decrease in matric suction is defined by shifting the Mohr–Coulomb (M-C) failure envelope towards compressive stress space during rainfall/runoff infiltration. Based on the proposed local shear strength method, the variable matric suction obtained from the bidirectionally coupled runoff and seepage analysis in FEM is unidirectionally transferred to the variable local shear strength for each soil material point in MPM (i.e., this is a FEM-MPM hybrid coupled model). Then, the correctness of the proposed hybrid coupled hydro-mechanical framework is effectively verified by a hypothetical homogeneous slope model. The results show that the slope stable/unstable state simulated by the proposed hybrid coupled hydro-mechanical framework has a good consistency with that simulated by the shear strength reduction technique (SSRT) and limit-equilibrium method (LEM). Afterward, combined with a case study of a natural landslide in Hokkaido, Japan, it is proved to be effective for simulating landslide runout subjected to rainfall/runoff infiltration by using the proposed hybrid coupled hydro-mechanical framework in an unsaturated soil slope.
Article
In addition to obvious negative effects on water quality in eutrophic aquatic ecosystems, recent work suggests that cyanobacterial harmful algal blooms (CHABs) also impact air quality via emissions carrying cyanobacterial cells and cyanotoxins. However, the environmental controls on CHAB-derived aerosol and its potential public health impacts remain largely unknown. Accordingly, the aims of this study were to 1) investigate the occurrence of microcystins (MC) and putatively toxic cyanobacterial communities in particulate matter ≤ 2.5 μm in diameter (PM2.5), 2) elucidate environmental conditions promoting their aerosolization, and 3) identify associations between CHABs and PM2.5 concentrations in the airshed of the Chowan River-Albemarle Sound, an oligohaline, eutrophic estuary in eastern North Carolina, USA. In summer 2020, during peak CHAB season, continuous PM2.5 samples and interval water samples were collected at two distinctive sites for targeted analyses of cyanobacterial community composition and MC concentration. Supporting air and water quality measurements were made in parallel to contextualize findings and permit statistical analyses of environmental factors driving changes in CHAB-derived aerosol. MC concentrations were low throughout the study, but a CHAB dominated by Dolichospermum occurred from late June to early August. Several aquatic CHAB genera recovered from Chowan River surface water were identified in PM2.5 during multiple time points, including Anabaena, Aphanizomenon, Dolichospermum, Microcystis, and Pseudanabaena. Cyanobacterial enrichment in PM2.5 was indistinctive between subspecies, but at one site during the early bloom, we observed the simultaneous enrichment of several cyanobacterial genera in PM2.5. In association with the CHAB, the median PM2.5 mass concentration increased to 8.97 μg m⁻³ (IQR = 5.15), significantly above the non-bloom background of 5.35 μg m⁻³ (IQR = 3.70) (W = 1835, p < 0.001). Results underscore the need for highly resolved temporal measurements to conclusively investigate the role that CHABs play in regional air quality and respiratory health risk.
Preprint
Full-text available
NON FORMATED PUBLISHED VERSION Feedbacks between climate change and eutrophication: revisiting the allied attack concept and how to strike back Despite its well-established negative impacts on society and biodiversity, eutrophication continues to be one of the most pervasive anthropogenic influence along the freshwater to marine continuum. The interaction between eutrophication and climate change, particularly climate warming, was explicitly focused upon a decade ago in the paper by Moss et al. (2011), which called for an integrated response to both problems, given their apparent synergy. In this review, we summarise advances in the theoretical framework and empirical research on this issue and analyse the current understanding of the major drivers and mechanisms by which climate change can enhance eutophication, and vice versa, with a particular focus on shallow lakes. Climate change can affect nutrient loading, through changes at the catchment and landscape levels by affecting hydrological patterns and fire frequency, and through temperature effects on nutrient cycling. Biotic communities and their interactions can also be directly and indirectly affected by climate change, leading to an overall weakening of resilience to eutrophication impacts. Increasing empirical evidence now indicates several mechanisms by which eutrophying aquatic systems can increasingly act as important sources of greenhouse gases to the atmosphere, particularly methane. We also highlight potential feedbacks between eutrophication, cyanobacterial blooms, and climate change. Facing both challenges at the same time is more pressing than ever. Meaningful and strong measures at the landscape and water body levels are therefore required if we are to ensure ecosystem resilience and safe water supply, conserving biodiversity, and decreasing the carbon footprint of freshwaters.
Article
Climate change may dramatically increase nitrate (NO3⁻) production and transport from watersheds to the coastal area due to short-term heavy precipitation events. However, the response of the coastal filter to such pulse NO3⁻ delivery is poorly studied. We measured NO3⁻ reduction rates via denitrification and DNRA in intact sediments collected from the Goro Lagoon (Po River Delta, Italy). We contrasted 2 seasons (spring and summer) and 2 sites (with lower and higher than average lagoon salinity). We performed ¹⁵NO3⁻ additions along a concentration series (50–2000 μM) far exceeding the annual NO3⁻ variations (20–150 μM) to quantify nitrate reduction saturation thresholds. In both seasons and sites denitrification largely outcompeted DNRA and increased along the NO3⁻ gradient, following Michaelis-Menten kinetics. At the site characterized by low salinity, maximum potential denitrification rates decreased from spring to summer, following the decrease in the abundance of burrowing macrofauna. DNRA followed the same seasonal trend but was not affected by NO3⁻ addition. At the site characterized by high salinity, denitrification rates slightly increased and DNRA decreased from spring to summer, despite the establishment of chemically reduced conditions and the increase in pore water free sulfides concentration. The Goro Lagoon sediments displayed elevated buffering capacity against NO3⁻ pulse additions. Such buffer capacity was mainly supported by denitrification through spring bioturbation, decreased summer pathlength of NO3⁻ to the anoxic zone, and unknown mechanisms preventing sulfide toxicity and the dominance of DNRA at the high salinity site.
Article
Despite its well-established negative impacts on society and biodiversity, eutrophication continues to be one of the most pervasive anthropogenic influence along the freshwater to marine continuum. The interaction between eutrophication and climate change, particularly climate warming, was explicitly focused upon a decade ago in the paper by Moss et al. (2011), which called for an integrated response to both problems, given their apparent synergy. In this review, we summarise advances in the theoretical framework and empirical research on this issue and analyse the current understanding of the major drivers and mechanisms by which climate change can enhance eutophication, and vice versa, with a particular focus on shallow lakes. Climate change can affect nutrient loading, through changes at the catchment and landscape levels by affecting hydrological patterns and fire frequency, and through temperature effects on nutrient cycling. Biotic communities and their interactions can also be directly and indirectly affected by climate change, leading to an overall weakening of resilience to eutrophication impacts. Increasing empirical evidence now indicates several mechanisms by which eutrophying aquatic systems can increasingly act as important sources of greenhouse gases to the atmosphere, particularly methane. We also highlight potential feedbacks between eutrophication, cyanobacterial blooms, and climate change. Facing both challenges at the same time is more pressing than ever. Meaningful and strong measures at the landscape and water body levels are therefore required if we are to ensure ecosystem resilience and safe water supply, conserving biodiversity, and decreasing the carbon footprint of freshwaters.
Article
Full-text available
Extreme weather events such as tropical storms and hurricanes deliver large amounts of freshwater (stormwater and river discharge) and associated dissolved organic carbon (DOC) to estuaries and the coastal ocean, affecting water quality, and carbon budgets. Hurricane Harvey produced an unprecedented 1000-year flood event in 2017 that inundated the heavily urbanized and industrialized Houston/Galveston region (TX, United States). Within a week, storm-associated floodwater delivered 87 ± 18 Gg of terrigenous dissolved organic carbon (tDOC) to Galveston Bay and the Gulf of Mexico continental shelves. In situ decay constants of 8.75–28.33 year−1 resulted in the biomineralization of ∼70% of tDOC within 1 month of discharge from the flood plain. The high removal efficiency of tDOC was linked to a diverse microbial community capable of degrading a wide repertoire of dissolved organic matter (DOM), and suggested hurricane-induced flood events affect net CO2 exchange and nutrient budgets in estuarine watersheds and coastal seas.
Article
Full-text available
Flooding from extreme weather events (EWE), such as hurricanes, exports large amounts of dissolved organic matter (DOM) to both estuaries and coastal waters globally. Hydrologic connectivity of wetlands to adjacent river channels during flood events can potentially have a major control on the DOM exported to coastal waters after EWEs. In this study, a geographic information system based flood model was used to: (1) determine the volume of flooded wetlands in a river corridor following Hurricane Matthew in 2016; (2) compute the resulting volume fluxes of DOM to the Neuse River Estuary-Pamlico Sound (NRE-PS), in eastern North Carolina and (3) use the flood model to quantify the wetland contribution to DOM export. The flood model-derived contributions were validated with a Bayesian Monte Carlo mixing model combining measurements of DOM quality: specific UV Absorbance at 254 nm (SUVA254), spectral slope ratio (SR), and stable isotope ratios of dissolved organic carbon (δ13C-DOC). Results indicated that (1) hydrologic connectivity of the freshwater riparian wetlands caused the wetlands to become the primary source of organic matter (OM) that was exported into the NRE-PS after Matthew and (2) this source lingered in these coastal waters in the months after the storm. Thus, in consideration of the pulse-shunt concept, EWE such as Hurricane Matthew cause pulses of DOM from wetlands, which were the primary source of the OM shunted from the terrestrial environment to the estuary and sound. Wetlands constituted ca. 48% of the annual loading of DOC into the NRE and 16% of DOC loading into the PS over a period of 30 days after Hurricane Matthew. Results were consistent with prior studies in this system, and other coastal ecosystems, that attributed a high reactivity of DOM as the underlying reason for large CO2 releases following EWE. Adapting the pulse-shunt concept to estuaries requires the addition of a “processing” step to account for the DOM to CO2 dynamics, thus a new pulse-shunt process is proposed to incorporate coastal waters. Our results suggest that with increasing frequency and intensity of EWE, strengthening of the lateral transfer of DOM from land to ocean will occur and has the potential to greatly impact coastal carbon cycling.
Article
Full-text available
Riverine dissolved organic matter (DOM) is a major source of reduced carbon exported from land to marine environments, and the inflow of riverine organic matter greatly affects biogeochemical cycling in estuaries and bays. Thus, any change in DOM composition, such as changes caused by flood waters as a result of storms and hurricanes, can subsequently affect estuarine environments. To investigate the impact of high flow events on riverine DOM, multidimensional molecular level information on DOM from four South Texas Rivers (Aransas, Lavaca, Mission, and Nueces Rivers) was acquired using high-resolution Ion Mobility Quadrupole Time of Flight Liquid Chromatography Mass Spectrometry (IM Q-TOF LCMS). Base-flow samples were collected in May, July, and October of 2016, June of 2017, and March of 2018, while high-flow samples were collected in September of 2017, as well as June and September of 2018. Based on the molecular formulas assigned from IM Q-TOF LCMS, the H/C ratio decreased during high-flow events (1.52 to 1.51 in ESI+ and 1.19 to 1.07 in ESI−), while the O/C ratio increased (0.31 to 0.33 in ESI−). Furthermore, DOM shifted from a protein-like and lipid-like dominated community at base flow conditions, to a lignin, tannin and condensed aromatic structure dominated community during high flow events, based on MS and tandem MS data. These changes in high-flow riverine DOM indicate an increase of terrestrial signal, which is likely a result of mobilization of terrestrial organic matter from the watersheds by flooding. The mobilized DOM, though refractory at high-flow conditions in rivers, could be reactive in coastal regions when conditions change, and thus could potentially fuel microbial activities downstream. In addition, about 3.76–21.8% of DOM molecules contain structural isomers among different flow conditions. This low number of isomer percentages suggests that DOM, as the products of various enzymatic biochemical reactions, is constrained in the number of isomers. Taken together, results from our study provide insights into structural changes of riverine DOM in response to extreme climate events in subtropical regions and have implications in understanding biogeochemical changes in estuaries under a changing climate.
Article
Full-text available
Coastal North Carolina, USA, has experienced three extreme tropical cyclone-driven flood events since 1999, causing catastrophic human impacts from flooding and leading to major alterations of water quality, biogeochemistry, and ecological conditions. The apparent increased frequency and magnitudes of such events led us to question whether this is just coincidence or whether we are witnessing a regime shift in tropical cyclone flooding and associated ecosystem impacts. Examination of continuous rainfall records for coastal NC since 1898 reveals a period of unprecedentedly high precipitation since the late-1990’s, and a trend toward increasingly high precipitation associated with tropical cyclones over the last 120 years. We posit that this trend, which is consistent with observations elsewhere, represents a recent regime shift with major ramifications for hydrology, carbon and nutrient cycling, water and habitat quality and resourcefulness of Mid-Atlantic and possibly other USA coastal regions.
Article
Full-text available
Dissolved organic matter (DOM) is a large and complex mixture of compounds with source inputs that differ with location, season, and environmental conditions. Here, we investigated drivers of DOM composition changes in a marsh‐dominated estuary off the southeastern United States. Monthly water samples were collected at a riverine and estuarine site from September 2015 to September 2016, and bulk, optical, and molecular analyses were conducted on samples before and after dark incubations. Results showed that river discharge was the primary driver changing the DOM composition at the mouth of the Altamaha River. For discharge higher than ~150 m3/s, dissolved organic carbon (DOC) concentrations and the terrigenous character of the DOM increased approximately linearly with river flow. For low discharge conditions, a clear signature of salt marsh‐derived compounds was observed in the river. At the head of Sapelo Sound, changes in DOM composition were primarily driven by river discharge and possibly by summer algae blooms. Microbial consumption of DOC was larger during periods of high discharge at both sites, potentially due to the higher mobilization and influx of fresh material to the system. The Georgia coast was hit by Hurricane Matthew in October 2016, which resulted in a large input of carbon to the estuary. The DOC concentration was ~2 times higher and DOM composition was more aromatic with a stronger terrigenous signature compared to the seasonal maximum observed earlier in the year during peak river discharge conditions. This suggests that extreme events notably impact DOM quantity and quality in estuarine regions.
Article
Full-text available
Plain Language Summary Recent hurricanes along the Southeastern and Gulf coasts of the United States have received much attention, because these extreme events have led to immense societal and economic impacts. Wetlands in coastal watersheds store large amounts of organic matter and upon flooding during extreme weather events are poised to release this material into adjacent rivers and estuaries where its decomposition can generate carbon dioxide. Alteration of carbon balances in these events can shift impacted coastal ecosystems from states of carbon sinks to carbon sources for periods of weeks to months. Understanding the balance between these states is important to our understanding of how, and how long, regional carbon cycling is impacted after such extreme weather events. A biweekly record of dissolved and particulate organic matter quantity and quality from a coastal watershed in North Carolina in the 3 months following Hurricane Matthew in 2016 illustrated a major input of wetland carbon to coastal waters caused by this storm and its substantial lingering effect on coastal carbon cycling.
Article
Full-text available
Coastal North Carolina (USA) has experienced 35 tropical cyclones over the past 2 decades; the frequency of these events is expected to continue in the foreseeable future. Individual storms had unique and, at times, significant hydrologic, nutrient-, and carbon (C)-loading impacts on biogeochemical cycling and phytoplankton responses in a large estuarine complex, the Pamlico Sound (PS) and Neuse River Estuary (NRE). Major storms caused up to a doubling of annual nitrogen and tripling of phosphorus loading compared to non-storm years; magnitudes of loading depended on storm tracks, forward speed, and precipitation in NRE-PS watersheds. With regard to C cycling, NRE-PS was a sink for atmospheric CO2 during dry, storm-free years and a significant source of CO2 in years with at least one storm, although responses were storm-specific. Hurricane Irene (2011) mobilized large amounts of previously-accumulated terrigenous C in the watershed, mainly as dissolved organic carbon, and extreme winds rapidly released CO2 to the atmosphere. Historic flooding after Hurricanes Joaquin (2015) and Matthew (2016) provided large inputs of C from the watershed, modifying the annual C balance of NRE-PS and leading to sustained CO2 efflux for months. Storm type affected biogeochemical responses as C-enriched floodwaters enhanced air–water CO2 exchange during ‘wet’ storms, while CO2 fluxes during ‘windy’ storms were largely supported by previously-accumulated C. Nutrient loading and flushing jointly influenced spatio-temporal patterns of phytoplankton biomass and composition. These findings suggest the importance of incorporating freshwater discharge and C dynamics in nutrient management strategies for coastal ecosystems likely to experience a stormier future.
Article
River systems worldwide have become substantially influenced by human activities, including land use changes, river diversion operations, and flood control measures. Some of the unambiguous and best studied examples of effects of enhanced eutrophication on biotic resources can be found in Louisiana estuaries at the terminus of the Mississippi-Atchafalaya River system. The Mississippi River delta has experienced large losses of coastal wetlands due to a combination of human impacts and sea-level rise. State and Federal agencies are moving ahead with plans for building large-scale river sediment diversions, which will capture maximum sediment during spring flood pulses and direct a sediment subsidy into the eroding coastal basins. These large-scale river sediment diversions will also substantially increase freshwater and nutrient inputs and are likely to affect algal bloom formation, including harmful cyanobacterial blooms. There are concerns that discharge of river water containing high concentrations of N, P and Si may trigger algal blooms in the coastal receiving basins. River sediment diversions, as any other flood pulsing, will likely be disruptive to the coastal ecology and so balancing the benefits of slowing coastal land loss against potential negative effects on water quality remains a formidable management challenge. We review here the physical, chemical and biological factors affecting primary production in shallow coastal systems and provide known data on ecosystem response to freshwater diversions, large and small. We also discuss potential management approaches to mitigate the negative impacts of the diversions on the health and stability of the coastal food webs.
Article
As the interface between riverine and coastal systems, estuaries play a key role in receiving, transporting, and processing terrestrial organic carbon prior to export to downstream coastal systems. Estuaries can switch from terrestrial organic carbon reactors under low river flow to pipelines under high flow, but it remains unclear how estuarine terrestrial organic carbon processing responds to the full spectrum of discharge conditions, which are bracketed by these high and low discharge events. The amount of terrestrial dissolved organic carbon and colored dissolved organic matter imported, processed, and exported was assessed for riverine discharge events spanning from the 4th to 99th flow quantiles in the Neuse River Estuary, North Carolina, USA using spatially and temporally (July 2015–December 2016) resolved measurements. The extent of dissolved organic matter processing in the estuary under various flow conditions was estimated using a non-steady state box model to calculate estuary-wide terrestrial dissolved organic carbon and colored dissolved organic matter source & sink terms. Under mid-range riverine discharge conditions (4th to 89th flow quantiles), the Neuse River Estuary was a sink for terrestrial dissolved organic carbon, retaining and/or processing (i.e., flocculation; photochemical and microbial degradation) on average ∼29% of terrestrial dissolved organic carbon. Following floods due to extreme precipitation events (99th flow quantile), however, over 99% of the terrestrial dissolved organic carbon loaded from the riverine end-member was exported directly to the downstream coastal system. Following such extreme weather events, the estuary acts as a pipeline for direct export of terrestrial dissolved organic carbon, drastically altering the amount and quality of dissolved organic carbon loaded to downstream coastal systems. This has important implications under future climate scenarios, where extreme weather events are expected to increase.