Measuring Changes in Consumer Resource Availability to Riverine Pulsing in Breton Sound, Louisiana, USA

Abstract

Resource pulses are thought to structure communities and food webs through the assembly of consumers. Aggregated consumers represent a high quality resource subsidy that becomes available for trophic transfer during and after the pulse. In estuarine systems, riverine flood pulses deliver large quantities of basal resources and make high quality habitat available for exploitation by consumers. These consumers represent a change in resources that may be available for trophic transfer. We quantified this increased consumer resource availability (nekton density, biomass, energy density) provided by riverine flood pulsing in Breton Sound, Louisiana, USA. We used water level differences between an area subject to two experimental riverine flood pulses (inflow) and a reference area not receiving inflow to identify the percentage of nekton standing stock and energy density that may be attributable solely to riverine pulsing and may represent a consumer resource subsidy. Riverine pulsing accounted for more than 60% of resident nekton density (ind m(-2)), biomass (g m(-2)), and energy density (cal m(-2)) on the flooded marsh surface during two experimental pulse events in 2005. Our results document the potential subsidy of resident nekton standing stock from a riverine flood pulse available for export to subtidal habitats. Given predicted large scale changes in river discharge globally, this approach could provide a useful tool for quantifying the effects of changes in riverine discharge on consumer resource availability.

Full text

Measuring Changes in Consumer Resource Availability to
Riverine Pulsing in Breton Sound, Louisiana, USA
Bryan P. Piazza
1
*
¤
, Megan K. La Peyre
2
1School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, Louisiana, United States of America, 2U.S. Geological Survey,
Louisiana Fish and Wildlife Cooperative Research Unit, School of Renewable Natural Resources, Louisiana State University Agricultural Center, Baton Rouge, Louisiana,
United States of America
Abstract
Resource pulses are thought to structure communities and food webs through the assembly of consumers. Aggregated
consumers represent a high quality resource subsidy that becomes available for trophic transfer during and after the pulse.
In estuarine systems, riverine flood pulses deliver large quantities of basal resources and make high quality habitat available
for exploitation by consumers. These consumers represent a change in resources that may be available for trophic transfer.
We quantified this increased consumer resource availability (nekton density, biomass, energy density) provided by riverine
flood pulsing in Breton Sound, Louisiana, USA. We used water level differences between an area subject to two
experimental riverine flood pulses (inflow) and a reference area not receiving inflow to identify the percentage of nekton
standing stock and energy density that may be attributable solely to riverine pulsing and may represent a consumer
resource subsidy. Riverine pulsing accounted for more than 60% of resident nekton density (ind m
22
), biomass (g m
22
), and
energy density (cal m
22
) on the flooded marsh surface during two experimental pulse events in 2005. Our results document
the potential subsidy of resident nekton standing stock from a riverine flood pulse available for export to subtidal habitats.
Given predicted large scale changes in river discharge globally, this approach could provide a useful tool for quantifying the
effects of changes in riverine discharge on consumer resource availability.
Citation: Piazza BP, La Peyre MK (2012) Measuring Changes in Consumer Resource Availability to Riverine Pulsing in Breton Sound, Louisiana, USA. PLoS ONE 7(5):
e37536. doi:10.1371/journal.pone.0037536
Editor: Martin Krkosek, University of Otago, New Zealand
Received July 21, 2011; Accepted April 24, 2012; Published May 30, 2012
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for
any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Funding: This work was funded by grants from the Louisiana Governor’s Applied Coastal Research and Development Program (LACRDP), the Coastal Restoration
and Enhancement through Science and Technology (CREST; www.gulfcrest.org) Program and by the Louisiana Department of Wildlife and Fisheries. The use of
trade, product, industry or firm names, or products is for informative purposes only and does not constitute an endorsement by the U.S. Government or the U.S.
Geological Survey. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: bpiazza@tnc.org
¤ Current address: The Nature Conservancy, Baton Rouge, Louisiana, United States of America
Introduction
Resource pulses affect many terrestrial and aquatic systems and
are thought to structure communities and food webs through the
assembly of consumers, particularly generalist species [1–5].
Aggregated consumers represent a resource subsidy that becomes
available for trophic transfer during and after the pulse. Several
examples provide evidence of allochthonous resource subsidies
propagating through secondary consumers in terrestrial and
aquatic systems [6–11], yet there are few studies that document
the value of the change in consumer resource availability that is
made available by an estuarine resource pulse [12].
Estuaries are pulsing ecosystems that receive periodic cross-
border subsidies of both marine and terrestrial origin [13–14].
One example of a marine resource pulse is that of migrating
anadromous fish. Tremendous amounts of allochthonous energy
are made available to the estuary annually by decomposing fish
carcasses, and this nutrient energy can be tracked through the food
web as consumers exploit the subsidy [15–17]. One of the most
influential pulses affecting community structure and function in
estuaries is freshwater inflow [13,18–19]. Freshwater inflow
delivers basal (terrestrial) resources to large expanses of estuarine
habitat and also makes high-quality habitat available for
exploitation by consumers that rapidly assemble to flooded
habitats. These consumers represent a measurable resource
subsidy that will become available to higher-order pelagic
consumers after the pulse ends [13,20]. In estuarine ecology, it is
generally accepted that resident nekton species may be critical in
this transfer and outwelling of energy across habitat boundaries
and to near-shore systems through a process known as trophic
relay (vascular plant material – microbes – invertebrates – fish,
[10,20–23]). Measuring the standing stock of these aggregated
resident nekton during riverine flood pulses may provide a means
to quantify the effects of the resource pulse and the resulting
consumer subsidy available for trophic transfer to pelagic habitats.
Freshwater pulses can occur with large runoff events, but more
often these pulses are the result of annual riverine flooding.
Riverine flood pulses deliver large quantities of allochthonous
resources to estuaries [24]. These resources are readily assimilated
by secondary consumers [12,25–28] and may be responsible for
increased nekton growth, changes in community structure, and
trophic diversity [28–31]. Riverine pulses are particularly impor-
tant for recruitment of resident nekton consumers that key into
these flood events for spawning and rapid growth [21,29–30,32].
Flood pulses in estuaries are highly variable, because they are
dependent on factors that are often far removed from the estuary
PLoS ONE | www.plosone.org 1 May 2012 | Volume 7 | Issue 5 | e37536

itself [33]. Flood pulses are driven both by variability in climate
(e.g., ENSO, climate change) and land use (e.g., dams, water
withdrawals) that affect flow [19,31,34–36], and future forecasts of
climate warming and increased development predict large scale
changes in river discharge on every continent [36]. This additional
variability in river flow will necessitate more management
interventions and restoration to protect ecosystems [31,36].
Consequently, there is a demand for greater basic understanding
of the value of riverine flood pulses for communities and food
webs, because attempts to protect estuarine systems will have to
include the maintenance and restoration of riverine flood pulses,
including their inherent variability.
Direct measures of consumer aggregation (e.g., density,
biomass, diversity, growth), and behavioral response (e.g., diet
switching, trophic cascade effects) are commonly used to assess the
effects of resource pulses on community and food-web dynamics
[1,4–6,28–30,32]. Although extremely valuable, these approaches
fail to provide high-level production measures, such as energy
density, that can be used for comparisons of habitat quality [37].
With this work, we propose to quantify the potential subsidy
(nekton density, biomass, energy density) provided by riverine
pulse events. We hypothesized that a riverine pulse event would
increase consumer resource availability, providing a positive
potential subsidy of nekton density, biomass and energy density.
We use the term ‘‘potential’’ because we are measuring what
might be available for actual transfer via predation, mortality,
excretion (i.e., consumer resource availability) and, in this study,
do not document actual transfer.
Methods
Ethics Statement
This work was conducted in accordance with institutional,
national and international guidelines concerning the use of
animals in research. The experimental protocol prepared for this
study was approved by the Louisiana State University Institutional
Animal Care and Use Committee – approval ID #05-008.
Study Area
The study took place in upper Breton Sound estuary, Louisiana,
USA, a 271,000 ha estuary in the Mississippi River deltaic plain of
southeast Louisiana (Fig. 1). It is microtidal and consists of bays,
lakes, bayous, canals, and fresh, intermediate, brackish, and saline
marsh types, and a relict Mississippi River distributary (Bayou
Terre aux Boeufs) that divides the basin geographically and
hydrologically. Dominant emergent vegetation in upper Breton
Sound consists of Spartina patens (Aiton) Muhl (Saltmeadow
cordgrass) and Schoenoplectus americanus (Pers.) Volkart ex Schizz &
R. Keller (Chairmaker’s bulrush).
The Caernarvon Freshwater Diversion structure is located at
the head of the estuary and is capable of delivering substantial
amounts of fresh water (227 m
3
s
21
), allochthonous sediments
(1610
8
kg y
21
) and nutrients to the basin [24,38]. Caernarvon
became operational in 1992 and was designed to moderate
salinities and reintroduce controlled river inflows to Breton Sound.
These controlled pulses release large fluxes of river water into the
basin and are capable of inundating upper basin marshes west of
Bayou Terre Aux Boeufs (,5,700 ha; inflow area) for several days
[32,38–39]. Furthermore, upper basin marshes east of Bayou
Terre Aux Boeufs are hydrologically separated from Caernarvon
flow, and flooding there is dominated by meteorological forcing,
providing a reference area subject only to flooding from
meteorological forcing [26]. The ability to control inflow provided
a unique opportunity to measure potential consumer resource
subsidies, because it allowed for experimental flood pulses with
control over the timing and duration of habitat flooding; the
presence of adjacent habitat hydrologically separated from the
inflow provided a reference area.
In this estuary, direct measures of consumer aggregation (e.g.,
density, biomass, diversity, growth), and behavioral response (e.g.,
diet switching, trophic cascade effects) have been shown to differ
between the inflow and reference areas, and these effects have
been attributed to riverine pulses through Caernarvon [25–26,28–
30,32]. However, up to now, no quantitative estimates have been
made of the potential energetic contribution of Caernarvon to
secondary production in Breton Sound estuary.
Data Collection
Nekton and environmental variables. Nekton samples and
environmental variables were collected daily through two exper-
imental riverine pulses in 2005 (February 14–28, March 12–28).
Each day, sampling locations were selected randomly within the
inflow area. Samples were collected with a 1.14-m cylindrical
(1 m
2
) drop sampler in vegetated marsh habitat located in marshes
downstream of the Caernarvon diversion structure. The drop
sampler was suspended approximately 3 m from the bow of the
boat and 1 m above the marsh surface by a telescoping aluminum
boom. A drop sampler was chosen because it provides many
advantages for sampling flooded marsh habitat including effec-
tiveness at cutting through underground plant runners, high catch
efficiency, and complete enclosure of the water column [40]. In
addition, the telescoping boom allowed sampling in the flooded
marsh 2–3 m from the edge where most nekton biomass on the
marsh surface occurs [41]. Each sampling site was approached
slowly and quietly. The outboard motor was shut off, and the boat
was allowed to drift to the vegetated marsh edge. In areas that
were too shallow to drift, investigators quietly pushed the boat into
position. Once in position, the sampler was dropped and seated
securely into the marsh substrate.
After the sampler was dropped, the location of the sampler was
logged with a Garmin GPS III, and a suite of environmental
variables was collected inside the sampler. Water temperature
(uC), conductivity (ms), salinity (psu), dissolved oxygen (DO, mg
l
21
), and pH were measured with a handheld YSI 556 MPS (YSI
Environmental, Inc.). Turbidity (NTU) was measured with a
fluorometer (Aquaflour 8000, Turner Designs, Inc.). Five water
depth measurements (mm) were taken inside the sampler with a
meter stick, and hourly water depth was downloaded from nearby
recorders (Inflow area – USGS 073745253, http://waterdata.usgs.
gov/usa/nwis/uv?site_no = 073745253; Reference area – USGS
073745257, http://waterdata.usgs.gov/nwis/
uv?format = gif&period = 31&site_no = 073745257). Percent vege-
tative composition of emergent vegetation was visually estimated
inside the sampler, and stems were clipped at the substrate and
returned to the lab where they were identified and sorted by
species and counted.
After environmental variables were measured, nekton inside the
drop sampler were collected with 10 successive dip net sweeps (in
opposite directions) by two investigators concurrently. After dip
netting, retained water was pumped through a 1-mm mesh
plankton net into a 1-mm mesh cod-end bag (Sea-Gear Corp.,
Melbourne, FL). Remaining organisms were removed from the
marsh substrate by hand. Organisms were preserved in 10%
formalin and returned to the laboratory for processing.
In the laboratory, samples were sorted, and nekton were
identified to the lowest feasible taxon and counted. Total length of
fish, shrimp, and crayfish and carapace width of crabs were
measured to the nearest mm. Individuals of each species in a
Pulse-Induced Nekton Subsidy
PLoS ONE | www.plosone.org 2 May 2012 | Volume 7 | Issue 5 | e37536

sample were pooled and weighed (g wet weight) to determine
biomass.
Nekton energy density and standing stock. Nekton
energy density of the six dominant species captured in 2005
sampling was determined using samples of these species collected
during a 2007 experimental flood pulse specifically for this
analysis. Because we only had wet weights from the 2005 sample
data, we needed to determine species specific energy density (cal
g
21
), and species specific wet:dry weight equations. Using dip nets,
individuals were collected weekly through an extended experi-
mental flood pulse in 2007 (January 26– March 12). Immediately
upon capture, nekton were frozen in an ice slurry and transported
back to the laboratory. Each individual was then measured (total
length, mm), weighed (wet weight, g), dried to a constant weight
(50uC, 48 h), and re-weighed (dry weight, DW g). For each species,
wet:dry weight equations were determined with simple linear
regression (Model dry weight = wet weight). Conspecifics from
each sample were pooled and pulverized. Analysis of energy
density was done on one gram DW nekton pellets (Parr model
2811 pellet press) with a Parr 6200 isoperibol oxygen bomb
calorimeter. Each pellet represented numerous individuals (.3) of
a particular species collected in a specific sample, and the number
of fish used for each pellet was dependent on the size of the
individuals caught. Three replicate pellets were analyzed for each
species and sample (i.e., date) combination if enough tissue powder
(3 g) was available. In the event that enough powder was not
available, we analyzed as many pellets as possible.
The standing stock nekton energy density was estimated using
the calculated energy density (above) of the six dominant resident
nekton species that assembled to flooded marsh habitat during
2005 flood pulse events (Palaemonetes paludosus,Heterandria formosa,
Gambusia affinis,Lucania parva,Poecilia latipinna,Cyprinodon variegatus,
[32]). Dry weight biomass (g m
22
) of each species in each 2005
sample was multiplied by its respective energy density (cal g
21
), as
calculated below, and then the product was summed to derive
specific energy density estimates (cal m
22
) for each 2005 sample.
This number represented the standing stock nekton energy per
square meter of flooded marsh surface in the inflow area during
2005 riverine flood pulses.
Nekton subsidy calculations. We defined the potential
nekton standing stock and energy density subsidies as the number
(ind m
22
), biomass (g m
22
), and energy density (cal m
22
) of nekton
present on the flooded marsh surface in the inflow area that
exceeded what would have been found without the freshwater
pulse event. To determine actual flooding that we could attribute
to the freshwater pulse, we used water levels in the reference area
as a guide to inform what water levels would have been in the
inflow area without the diversion, and this guide was used to
develop nekton subsidy calculations (described below). Specifically,
we used water level differences between the inflow and reference
Figure 1. Breton Sound estuary, Louisiana, USA and the inflow (light gray) and reference (dark gray) areas used in this study. Also
shown is the location of the Caernarvon Freshwater Diversion. Map adapted from [32,39].
doi:10.1371/journal.pone.0037536.g001
Pulse-Induced Nekton Subsidy
PLoS ONE | www.plosone.org 3 May 2012 | Volume 7 | Issue 5 | e37536

areas to identity the percentage of nekton standing stock and
energy density in inflow marshes that may represent a resource
subsidy provided by two experimental Caernarvon river pulses.
To quantify these subsidies, it was first necessary to separate
samples taken in the inflow area into subsidized and unsubsidized
categories. Subsidized samples were defined as those that met one
of the following two conditions. They were taken in the inflow area
either (1) when the reference area was not flooded, or (2) when the
reference area was flooded, but the mean water level in the inflow
area was greater than the maximum mean depth of flooding in the
reference area. This approach assumed that without the freshwa-
ter flow from Caernarvon, the upper inflow basin would have
flooded simultaneously to and with approximately the same
characteristics as the reference basin.
Next, we calculated estimates of the potential nekton subsidy for
each pulse event (February/March) by determining the proportion
of total nekton density, biomass, and nekton energy accounted for
by subsidized samples (i.e., X(subsidized samples)/X(total sam-
ples), where X = nekton density, biomass or energy density).
Finally, these proportions were averaged across pulses and then
multiplied by the mean density, biomass and energy estimates
from the inflow area to calculate estimates of nekton standing stock
(ind m
22
,gm
22
) and potential energy subsidy (cal m
22
) that could
be considered to be due to the riverine inflow.
Results
Nekton and Environmental Variables
A total of 141 samples were collected within the inflow area
during the pulse events. During sampling, salinity, temperature,
dissolved oxygen, and turbidity were within the normal range of
estuarine variability in this region (Table 1). Furthermore, during
sampling, the marsh was flooded 69% (February pulse) and 64%
(March pulse) of the time in the inflow area, and only 31%
(February pulse) and 14% (March pulse) of the time in the
reference area. Subsidized samples comprised 91% (n = 60) and
92% (n = 69) of the inflow samples collected in February and
March, respectively. Flooding in the reference area was driven
Figure 2. Water level and marsh elevations (National Geodetic Vertical Datum, NGVD) before and during two (February 14–28 and
March 12–28) Caernarvon experimental high-pulse flow events into Breton Sound estuary in 2005. Because the reference area did not
contain a surveyed water level recorder, stages and marsh level were based on an investigator-created datum, transferred from USGS 73745257
http://waterdata.usgs.gov/nwis/uv?format = gif&period = 31&site_no = 073745257; NGVD).
doi:10.1371/journal.pone.0037536.g002
Table 1. Environmental characteristics in inflow marshes
during two Caernarvon experimental high-flow pulses in
February and March 2005.
Variable February (n = 66) March (n = 75)
Salinity (psu) 0.360.01 (0.220.7) 0.260.01 (0.220.2)
Dissolved Oxygen (ppm) 5.760.22 (1.829.4) 2.260.08 (1.024.3)
Water Temperature (uC) 17.360.35 (11.3223.2) 18.460.50 (10.5228.1)
Turbidity (NTU) 15.961.14 (0.8250.0) 14.961.06 (0.9238.3)
Data are expressed as mean 6SE (range).
doi:10.1371/journal.pone.0037536.t001
Pulse-Induced Nekton Subsidy
PLoS ONE | www.plosone.org 4 May 2012 | Volume 7 | Issue 5 | e37536

solely by meteorological and tidal forcing during the time of
sampling; in contrast, the freshwater inflow obscured tidal
periodicity in the inflow area soon after diversion pulsing began
(Fig. 2).
A total of 5,948 individuals of 16 taxa were collected in the
inflow area during sampling. Six species – Palaemonetes paludosus
(n = 2,363), Heterandria formosa (n = 1,975), Gambusia affinis (n = 743),
Lucania parva (n = 377), Poecilia latipinna (n = 81), Cyprinodon variegatus
(n = 70) – comprised 95% of the total abundance and were
selected for use in calculations of nekton energy density.
Information on the total nekton community sampled can be
found in [32].
Nekton Energy Density and Standing Stock
A minimum of 24 individuals of each of the six dominant
species were caught in 2007 and used to determine energy density
and wet;dry weight regressions (Table 2). Regression analysis
revealed highly significant dry weight conversion equations for the
six dominant resident fish species, and mean water content of all
species was similar (78–81%). Energy density values for resident
nekton ranged from 5,410–6,718 cal g
21
, with highest mean
energy density reported for Heterandria formosa (Table 2).
Standing stock density of the six dominant resident nekton
species in inflow marshes ranged from 2.6–32.6 ind m
22
during
the freshwater pulses (Table 3). These assembled individuals
represented an available stock of transferrable energy on the
flooded marsh surface that ranged from 227.3–4215.7 cal m
22
.
During both pulses, standing stock of Palaemonetes paludosus was
greatest. There was also intraspecific variability in the available
standing stock between pulses. For example, standing stock density
of Heterandria formosa increased almost threefold, and its energy
density increased almost fourfold from February to March pulses.
Potential Nekton Energetic Subsidy
Subsidized samples represented 67.6617.1% of the standing
stock nekton density and 61.1612.1% of the nekton biomass in
the inflow marshes during the 2005 riverine flood pulses (Table 4).
Additionally, inflow marshes contained over 8,000 cal m
22
of
standing stock resident nekton energy, of which 61.7615.8% was
subsidized by the flood pulses.
Discussion
Managed riverine pulsing at the Caernarvon freshwater
diversion structure increased potential consumer resource avail-
ability by as much as 60% as measured by increased nekton
density, biomass, and energy density. These marshes receiving
freshwater pulses contained over 8,000 cal m
22
of standing-stock
resident nekton energy that was available for export and
assimilation by higher trophic levels as water levels receded. This
increase in consumer resource availability quantifies potential
subsidies that could contribute to system energetics via transfer
Table 2. Wet weight biomass (WW; g) to dry weight biomass (DW; g) relationships and mean energy density (cal g
21
DW) for six
dominant resident nekton species caught weekly on the flooded marsh surface in upper Breton Sound estuary, Louisiana
throughout an experimental riverine flood pulse in spring 2007.
Wet Weight - Dry Weight Energy Density
Species Common Name n Equation r
2
Mean (SE)
Water Content n (pellets)
Mean (SE)
cal g
21
DW
Palaemonetes paludosus Riverine grass shrimp 392 DW = 0.190571(WW) 0.81 0.81 (0.002) 181 (8) 6141.85 (45.01)
Heterandria formosa Least killifish 167 DW = 0.205544(WW) 0.66 0.81 (0.008) 146 (2) 6626.12 (7.48)
Gambusia affinis Mosquitofish 2193 DW = 20.002934+0.206633(WW) 0.91 0.81 (0.001) 921 (36) 6294.70 (48.42)
Lucania parva Rainwater killifish 80 DW = 20.01548+0.241053(WW) 0.90 0.81 (0.003) 60 (4) 5790.55 (204.37)
Poecilia latipinna Sailfin molly 164 DW = 20.005112+0.230281(WW) 0.98 0.78 (0.002) 46 (5) 6435.60 (49.51)
Cyprinodon variegatus Sheepshead minnow 39 DW = 20.014876+0.215689(WW) 0.99 0.81 (0.003) 24 (3) 5421.80 (9.99)
All relationships are statistically significant at p,0.0001. Equations with no intercept indicate that the intercept was not significantly different from zero.
doi:10.1371/journal.pone.0037536.t002
Table 3. Mean (6SE) standing stock nekton density (ind m
22
) and nekton energy density (cal m
22
) for the six dominant nekton
species that assembled to the flooded marsh surface in the inflow area during two (February and March 2005) experimental
riverine flood pulses in upper Breton Sound estuary, Louisiana.
February (n = 66) March (n = 75)
Species Common Name Density Energy Density Density Energy Density
Palaemonetes paludosus Riverine grass shrimp 28.865.3 4215.76765.8 15.264.2 3511.46936.6
Heterandria formosa Least killifish 12.462.4 590.46106.8 32.6611.8 2312.861058.3
Gambusia affinis Mosquitofish 11.263.6 700.76226.8 10.562.2 1511.66368.0
Lucania parva Rainwater killifish 8.562.5 1427.56397.2 3.260.5 537.86146.2
Poecilia latipinna Sailfin molly 2.960.7 293.16110.9 2.660.5 553.16168.1
Cyprinodon variegatus Sheepshead minnow 2.960.8 227.36126.1 2.960.5 446.66129.8
doi:10.1371/journal.pone.0037536.t003
Pulse-Induced Nekton Subsidy
PLoS ONE | www.plosone.org 5 May 2012 | Volume 7 | Issue 5 | e37536

through numerous mechanisms including predation, mortality, or
excretion [3,5–6,9].
While our approach was able to document an increase in
consumer resource availability, it did not identify the specific
underlying mechanism(s) (i.e., increased marsh access, increased
food supply) responsible for this. There is debate among estuarine
ecologists whether the positive effects of freshwater flow on
consumer populations are linked to bottom-up controls (e.g.,
Apalachicola Bay [42]), simply the change in physical habitat
attributes that occur with flooding (e.g., San Francisco Bay [43]),
or both. In this study, we were able to demonstrate clearly that
these Caernarvon pulses provide potential trophic subsidies, as
measured by nekton density, biomass and energy density that can
be attributed to flooding from the pulse event suggesting that
physical habitat changes may be one of the key mechanisms. This
finding is supported by past research in this system demonstrating
that increased nekton density and community changes are
associated with increased water levels during pulse events
[30,32] or changes in salinity [28,30]. At the same time, other
studies in this system demonstrate that these riverine flood pulses
deliver a significant amount of basal resources (140 mM of total N,
5mM total P) at a level that is directly comparable to other
allochthonous resource pulses in aquatic habitats (migratory
salmon, [8]; migratory waterfowl, [44]; cicada carcasses, [9]) and
that these nutrients are rapidly assimilated in the upper estuary
[24]. Studies in this estuary also show that riverine nutrients
propagate into the resident nekton consumers [25–26,28–29]
supporting the bottom-up control concept. However, we did not
quantify the actual transfer of this subsidy to the higher-order
consumers (i.e., predation). Combined, this evidence suggests that
both bottom-up control and change in physical habitat attributes
may play a role in impacting consumer resource availability;
however, we still lack specific evidence of actual trophic transfer
[25–26,28–30,32].
Several different models have been proposed to explain how
resource pulses structure communities and food webs (i.e. trophic
relay, onion model, spider web model, internet model, constant
connectance hypothesis; [21,45–46]). In this estuary, this study
and others suggest that a relatively small number of resident
species contribute disproportionately to changes in the food web,
which conceptually supports the simplified food web models (i.e.,
trophic relay; [25–26,28–30,32]). While this study showed that
relatively few resident species formed the core of the potential
energy available for trophic relay, we did not investigate actual
food web transfer. However, during this study we routinely
observed red drum (Sciaenops ocellatus), a species predominantly
found in brackish to marine waters, cruising alongside the flooded
marsh edge, outside their preferred salinity regime (salinity ,1.0;
[32]). These observations suggest that aggregated nekton on the
flooded marsh surface provided a high-enough quality food source
to lure them into a suboptimal environment. These observations
would appear to concur with other studies suggesting that under
seasonal (predictable) flood pulse regimes, some species will
tolerate sub-optimal conditions to exploit predictable resources
[47–48]. Future research on the effects of resource pulses should
be directed toward unraveling specific food-web interactions with
a combination of field sampling and experimental manipulation in
order to determine such things as the response of highly mobile
pelagic and avian predators [2,9,23], energy flow and interaction
between nekton consumers and invertebrate prey [22], lags in
assembly and nutrient transfer [9], and community response [2].
It has been suggested that aggregation represents only half of
the consumer response to resource pulses, and that reproduction
may have more persistent effects on local communities [2,5].
Resident nekton species, particularly poeciliids, have been shown
to be intimately tied to seasonally flooded wetland habitats in both
forested wetlands and coastal marshes, as spawning, and breeding
episodes typically coincide with flood events [21,49]. We did not
document reproductive status of resident nekton during riverine
pulse events; however, our energy density results suggest that
aggregated nekton may have been reproducing in flooded
marshes. Reproductive status has a disproportionate effect on
caloric value because the gonadal tissue is comprised largely of
lipids and contributes to high overall energy values during
reproduction [50–52]. Seasonal variability in energy density
corresponding to reproduction has been shown for clupeids
[15,51,53], salmonids [52], and gadids [54]. In poeciliids, it has
been shown that as Gambusia affinis females increase in size, energy
density increases, and the majority of the total energy is contained
in ovaries and developing embryos [50]. High energy values for
the nekton species in our study, particularly for Heterandria formosa,
may reflect the onset of breeding, as reproduction in estuarine
residents is particularly keyed to flooding events [21]. Future work
should involve an assessment of the reproductive status of
individuals during sampling.
While, clearly, actual nekton subsidy likely is affected by
characteristics and timing of the riverine pulsing, the density and
biomass values calculated for this study are directly comparable to
those reported in other wetland systems [26,55–56]; furthermore,
when expressed as percentages, the subsides calculated in this
study are similar to cross-border subsidies calculated in other
systems (e.g., terrestrial insect subsidies comprise 27–60% of prey
volume of some fish species [6]; terrestrial invertebrate prey
subsidies comprise ,50–70% of salmonid diets [11,57]). These
Table 4. Mean (SE) standing stock of resident nekton – density (ind m
22
), biomass (g DW m
22
), and energy density (cal m
22
)–
that assembled to the flooded marsh surface in the inflow area during two (February and March 2005) experimental riverine flood
pulses in upper Breton Sound estuary, Louisiana.
Nekton Subsidy
Mean (SE) in Inflow area % Mean (SE) attributed to resource pulse
Resident Nekton Density (ind m
22
) 40.0 (7.2) 67.6 27.0 (4.8)
Nekton Biomass (g DW m
22
) 1.3 (0.2)
1
61.1 0.8 (0.1)
Nekton Energy Density (cal m
22
) 8164.0 (1490.0) 61.7 4990.8 (895.6)
Also shown is the estimated nekton standing stock that was a subsidy attributed to the experimental pulses. Mean standing stock is based on nekton community data
reported in a previous study [32]. Dry weight biomass was calculated with equations in Table 2. Errors for potential nekton subsidy were calculated using the formula
(Z
err
= Z[(X
err
/X)
2
(Y
err
/Y)
2
]
1/2
.
doi:10.1371/journal.pone.0037536.t004
Pulse-Induced Nekton Subsidy
PLoS ONE | www.plosone.org 6 May 2012 | Volume 7 | Issue 5 | e37536

subsidy numbers were calculated for experimental spring pulses
that were designed to mimic historic seasonal flood pulses, and
thus possibly captured subsidies that reflect evolved responses
[48]. In contrast, aseasonal flood pulse regimes may not elicit
similar numbers or may require examination of different
species. Maintenance of natural flood patterns thus may be
critical in sustaining these subsidies and timing of managed flood
pulses may have important food web implications.
Energy density estimates may provide a meaningful and
comparable assessment of the energetic value of higher-order
resource subsidies. Although estimates of energy flow may be
inappropriate for understanding the effects of resource pulses on
community dynamics [58], gross energy content is not only a
useful measure of physiological status, health, and changes in
habitat quality but is also a high-level production-related measure
of the direct link between coastal marsh habitat and fishery
production [37,59–61]. Therefore, the potential energy density
subsidy may be a good measure of the effect of resource pulses on
habitat quality and a comparable measure of the change in
consumer resource availability that results from resource pulses.
Acknowledgments
S. Hillen (JHT Inc.) and L. Rozas (NOAA Fisheries) provided technical
assistance and field support. C. Cannaday, W. Cochran, B. Gossman, D.
King, C. Llewellyn, S. Piazza, A. Piehler, M. Piehler, S. Pierliuissi, and A.
Podey provided field assistance. M. Piehler and W. Gayle provided lab
assistance. J. Cowan and A. Fischer provided the bomb calorimeter. M.
Fisher provided the map figure. M. Benge, M. Farizo (Delacroix
Corporation) provided landrights, lodging, and support of LSU coastal
research. USGS National Wetlands Research Center provided lodging. C.
Villarubia (LDNR), T. Bernhard (LDNR), L. Serpas (Plaquemines Parish)
and the Caernarvon Interagency Advisory Committee provided experi-
mental freshwater pulses. B. Roth, G. Holm, and J. Trexler all provided
insightful comments that greatly enhanced this work.
Author Contributions
Conceived and designed the experiments: BP ML. Performed the
experiments: BP. Analyzed the data: BP. Contributed reagents/materi-
als/analysis tools: BP ML. Wrote the paper: BP ML.
References
1. Anderson WB, Wait DA, Stapp P (2008) Resources from another place and
time: responses to pulses in a spatially subsidized system. Ecology 89: 660–670.
2. Holt RD (2008) Theoretical perspectives on resource pulses. Ecology 89:
671–681.
3. NowlinWH, Vanni MJ, Yang LH (2008) Comparing resource pulses in aquatic
and terrestrial ecosystems. Ecology 89: 647–659.
4. Schmidt KA, Ostfeld RS (2008) Numerical and behavioral effects within a pulse-
driven system: consequences for shared prey. Ecology 89: 635–646.
5. Yang LH, Bastow JL, Spence KO, Wright AN (2008) What can we learn from
resource pulses? Ecology 89: 621–634.
6. Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape
and food web ecology: the dynamics of spatially subsidized food webs. Ann Rev
Ecol Syst 28: 289–316.
7. Yang LH (2004) Periodical cicadas as resource pulses in North American forests.
Science 306: 1565–1567.
8. Claeson SM, Li JL, Compton JE, Bisson PA (2006) Response of nutrients,
biofilm, and benthic insects to salmon carcass addition. Can J Fish Aquat Sci 63:
1230–1241.
9. Nowlin WH, Gonza´lez MJ, Vanni MJ, Henry M, Stevens H, et al. (2007)
Allochthonous subsidy of periodical cicadas affects the dynamics and stability of
pond communities. Ecology 88: 2174–2186.
10. Heck KL Jr., Carruthers TJB, Duarte CM, Hughes AR, Kendrick G, et al.
(2008) Trophic transfers from seagrass meadows subsidize diverse marine and
terrestrial consumers. Ecosystems 11: 1198–1210.
11. Eberle LC, Stanford JA (2010) Importance and seasona l availability of terrestrial
invertebrates as prey for juvenile salmonids in floodplain spring brooks of the
Kol River (Kamchatka, Russian Federation). River Res Applic 26: 682–694.
12. Schlacher TA, Connolly RM, Skillington AJ, Gaston TF (2009) Can export of
organic matter from estuaries support zooplankton in nearshore, marine
plumes? Aquat Ecol 43: 383–393.
13. Odum WE, Odum EP, Odum HT (1995) Nature’s pulsing paradigm. Estuaries
18: 547–555.
14. Howe ER, Simenstad CA (2007) Restoration trajectories and food web linkages
in San Francisco Bay’s estuarine marshes: a manipulative translocation
experiment. Mar Ecol Prog Ser 351: 65–76.
15. Durbin AG, Nixon SW, Oviatt CA (1979) Effects of the spawning migration of
the alewife, Alosa pseudoharengus, on freshwater ecosystems. Ecology 60: 8–17.
16. Naiman RJ, Bilby RE, Schindler DE, Helfield JM (2002) Pacific salmon,
nutrients, and the dynamics of freshwater and riparian ecosystems. Ecosystems
5: 399–417.
17. Brock CS, Leavitt PR, Schindler DE, Quay PD (2007) Variable effects of
marine-derived nutrients on algal production in salmon nursery lakes of Alaska
during the past 300 years. Limnol Oceanogr 52: 1588–1598.
18. Sklar FH, Browder JA (1998) Coastal environmental impacts brought about by
alterations to freshwater flow in the Gulf of Mexico. Environ Manage 22:
547–562.
19. Alber M (2002) A conceptual model of estuarine freshwater inflow management.
Estuaries 25: 1246–1261.
20. Odum EP (2000) Tidal marshes as outwelling/pulsing systems. In:
Weinstein MP, and Kreeger DA, eds. Concepts and controversies in tidal
marsh ecology. Kluwer Academic Publishers. Dordrecht, The Netherlands. pp
3–7.
21. Kneib RT (1997) The role of tidal marshes in the ecology of estuarine nekton.
Oceanogr Mar Biol Ann Rev 35: 163–220.
22. Connolly RM, Gorman D, Guest MA (2005) Movement of carbon among
estuarine habitats and its assimilation by invertebrates. Oecologia 144: 684–691.
23. Stevens PW, Montague CL, Sulak KJ (2006) Fate of fish production in
seasonally flooded saltmarsh. Mar Ecol Progr Ser 327: 267–277.
24. Lane RR, Day JW, Justic D, Reyes E, Marx B, et al. (2004) Changes in
stoichiometric Si, N and P ratios of Mississippi River water diverted through
coastal wetlands to the Gulf of Mexico. Estuar Coast Shelf Sci 60: 1–10.
25. Wissell B, Fry B (2005) Tracing Mississippi River influences in estuarine food
webs of coastal Louisiana. Oecologia 144: 659–672.
26. Rozas LP, Minello TJ, Munera-Ferna´ ndez I, Fry B, Wissel B (2005)
Macrofaunal distributions and habitat change following winter-spring releases
of freshwater into the Breton Sound estuary, Louisiana (USA). Estuar Coast
Shelf Sci 65: 319–336.
27. Connolly RM, Schlacher TA, Gaston TF (2009) Stable isotope evidence for
trophic subsidy of coastal benthic fisheries by river discharge plumes off small
estuaries. Mar Biol Res 5: 164–171.
28. de Mutsert K (2010) . The effects of a freshwater diversion on nekton species
biomass distributions, food web pathways, and community structure in a
Louisiana estuary. Ph.D. Dissertation. Louisiana State University, Baton Rouge,
Louisiana, USA.
29. Piazza BP, La Peyre MK (2010) Using Gambusia affinis growth and condition to
assess estuarine habitat quality: a comparison of indices. Mar Ecol Prog Ser 412:
231–245.
30. Piazza BP, La Peyre MK (2011) Nekton community response to a large-scale
Mississippi River discharge: examining spatial and temporal response to river
management. Estuar Coast Shelf Sci 91: 379–387.
31. Vinagre C, Salgado J, Cabral HN, Costa MJ (2011) Food web structure and
habitat connectivity in fish estuarine nurseries. Estuar Coast 34: 663–674.
32. Piazza BP, La Peyre MK (2007) Restoration of the annual flood pulse in Breton
Sound, Louisiana, USA: habitat change and nekton community response. Aquat
Biol 1: 109–119.
33. Gillanders BM, Kingsford MJ (2002) Impact of changes in flow of freshwater on
estuarine and open coastal habitats and the associated organisms. Oceanogr
Mar Biol Ann Rev 40: 233–309.
34. Junk, WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-
floodplain systems. In: Dodge DP, ed. Proceedings of the international large
river symposium Can Special Pub Fish Aqu Sci 106. pp. 110–127.
35. Lonerag an NR, Bunn SE (1999) River flows and estuarine ecosystems:
Implications for coastal fisheries from a review and a case study of the Logan
River, southeast Queensland. Austral J Ecol 24: 431–440.
36. Palmer MA, Reidy Liermann CA, Nilsson C, Flo¨ rke M, Alcamo J, et al. (2008)
Climate change and the world’s river basins: anticipating management options.
Front Ecol Environ 2008; 6: doi:10.1890/060148.
37. Zimmerman RJ, Minello TJ, Rozas LP (2000) Salt marsh linka ges to
productivity of penaeid shrimps and blue crabs in the northern Gulf of Mexico.
In: Weinstein MP, Kreeger, DA, eds. Concepts and controversies in tidal marsh
ecology Kluwer Academic Publishers, Dordrecht. pp. 293–314.
38. Snedden GA, Cable JE, Swarzenski C, Swenson E (2007) Sediment discharge
into a subsiding Louisiana deltaic estuary through a Mississippi River diversion.
Estuar Coast Shelf Sci 71: 181–193.
39. Snedden GA, Cable JE, Wiseman WJ (2007) Subtidal sea level variability in a
Mississippi River deltaic estuary, Louisiana. Estuar Coast 30: 802–812.
Pulse-Induced Nekton Subsidy
PLoS ONE | www.plosone.org 7 May 2012 | Volume 7 | Issue 5 | e37536

40. Rozas LP, Minello TJ (1997) Estimating densities of small fishes and decapod
crustaceans in shallow estuarine habitats: a review of sampling design with focus
on gear selection. Estuaries 20: 199–213.
41. Kneib RT (2000) Salt marsh ecoscapes and production transfers by estuarine
nekton in the southeastern United States. In: Weinstein MP, Kreeger, DA, eds.
Concepts and controversies in tidal marsh ecology Kluwer Academic Publishers,
Dordrecht. pp. 267–291.
42. Livingston RJ, Niu X, Lewis FG III, Woodsum GC (1997) Freshwater input to a
gulf estuary: long-term control of trophic organization. Ecol Appl 71: 277–299.
43. Kimmerer WJ (2002) Physical, biological, and management responses to
variable freshwater flow into the San Francisco estuary. Estuaries 25:
1275–1290.
44. Kitchell JF, Schindler DE, Herwig BR, Post DM, Olson MH, et al. (1999)
Nutrient cycling at the landscape scale: the role of diel foraging migrations by
geese at the Bosque del Apache National Wildlife Refuge, New Mexico. Limnol
Oceanogr 44: 828–836.
45. Winemiller KO, Layman CA (2005) Food web science: moving on the path from
abstraction to prediction. In: de Ruiter PC, Wolters V, Moore JC, eds. Dynamic
food webs: multispecies assemblages, ecosystem development and environmental
change, Elsevier, Amsterdam. pp 10–23.
46. Banasˇek-Richter C, Bersier LF, Cattin MF, Baltensperger R, Gabriel JP, et al.
(2009) Complexity in quantitative food webs. Ecology 90: 1470–1477.
47. Rutherford DA, Gelwicks KR, Kelso WE (2001) Physicochemical effects of the
flood pulse on fishes in the Atchafalaya River Basin, Louisiana. Trans Am Fish
Soc 130: 276–288.
48. Winemiller KO (2004) Floodplain riv er food webs: generalization s and
implications for fisheries management. In: Welcomme R, Petr T, eds.
Proceedings of the second international symposium on the management of
large rivers for fisheries, Vol II. RAP Publication 2004/17. pp 285–309.
49. Winemiller KO (1993) Seasonality of reproduction by livebea ring fishes in
tropical rainforest streams. Oecologia 93: 266–276.
50. Vondracek B, WurtsbaughWA, Cech JJ Jr. (1988) Growth and reproduction of
mosquitofish, Gambusia affinis, in relation to temperature and ration level:
consequences for life history. Env Biol Fish 21: 45–57.
51. Perez MA (1994) Calorimetry measurements of energy value of some Alaskan
fishes and squids. U.S. Dept Comm, NOAA Tech Memo NMFS-AFSC-32.
52. Jonsson B, Jonsson N (2005) Lipid energy reserves influence life-history decision
of Atlantic salmon (Salmo salar) and brown trout (S. trutta) in fresh water. Ecol
Freshwater Fish 14: 296–301.
53. Strange RJ, Pelton JC (1987) Nutrient content of clupeid forage fishes. T Am
Fish Soc 116: 60–66.
54. Pederson J, Hislop JRG (2001) Seasonal variations in the energy density of fishes
in the North Sea. J Fish Biol 59: 380–389.
55. Barletta M, Barletta-Bergen A, Saint-Paul U, Hubold G (2005) The role of
salinity in structuring the fish assemblages in a tropical estuary. J Fish Biol 66:
45–72.
56. Williams AJ, Trexler JC (2006) A preliminary analysis of the correlation of food-
web characteristics with hydrology and nutrient gradients in the southern
Everglades. Hydrobiologia 569: 493–504.
57. Kawaguchi Y, Nakano S (2001) Contribution of terrestrial invertebrates to the
annual resource budget for salmonids in forest and grassland reaches of a
headwater stream. Freshwater Biol 46: 303–316.
58. Polis GA, Strong DR (1996) Food web complexity and community dynamics.
Am Nat 147: 813–846.
59. Pangle KL, Sutton TM (2005) Temporal changes in the relationship between
condition indices and proximate composition of juvenile Coregonus artedi. J Fish
Biol 66: 1060–1072.
60. Wanless S, Harris MP, Redman P, Speakman JR (2005) Low energy values of
fish as a probable cause of a major seabird breeding failure in the North Sea.
Mar Ecol Prog Ser 294: 1–8.
61. Cianco J, Pascual M (2006) Energy density of freshwater Patagonian organisms.
Ecologı
´a Austral 16: 91–94.
Pulse-Induced Nekton Subsidy
PLoS ONE | www.plosone.org 8 May 2012 | Volume 7 | Issue 5 | e37536