BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-13-313-2016Carbon storage in seagrass soils: long-term nutrient history exceeds the
effects of near-term nutrient enrichmentArmitageA. R.armitaga@tamug.eduhttps://orcid.org/0000-0003-1563-8026FourqureanJ. W.Department of Marine Biology, Texas A&M University at
Galveston, Galveston, Texas, USADepartment of Biological Sciences and Southeast
Environmental Research Center, Florida International University, Miami,
Florida, USAA. R. Armitage (armitaga@tamug.edu)15January201613131332121August20152October20158December201515December2015This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/This article is available from https://bg.copernicus.org/articles/13/313/2016/bg-13-313-2016.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/13/313/2016/bg-13-313-2016.pdf
The carbon sequestration potential in coastal soils is linked to aboveground
and belowground plant productivity and biomass, which in turn, is directly
and indirectly influenced by nutrient input. We evaluated the influence of
long-term and near-term nutrient input on aboveground and belowground carbon
accumulation in seagrass beds, using a nutrient enrichment (nitrogen and
phosphorus) experiment embedded within a naturally occurring, long-term
gradient of phosphorus availability within Florida Bay (USA). We measured
organic carbon stocks in soils and above- and belowground seagrass biomass
after 17 months of experimental nutrient addition. At the nutrient-limited
sites, phosphorus addition increased the carbon stock in aboveground seagrass
biomass by more than 300 %; belowground seagrass carbon stock increased
by 50–100 %. Soil carbon content slightly decreased (∼ 10 %)
in response to phosphorus addition. There was a strong but non-linear
relationship between soil carbon and Thalassia testudinum leaf
nitrogen : phosphorus (N : P) or belowground seagrass carbon stock. When
seagrass leaf N : P exceeded an approximate threshold of 75:1, or when
belowground seagrass carbon stock was less than 100 g m-2, there was
less than 3 % organic carbon in the sediment. Despite the marked
difference in soil carbon between phosphorus-limited and phosphorus-replete
areas of Florida Bay, all areas of the bay had relatively high soil carbon
stocks near or above the global median of 1.8 % organic carbon. The
relatively high carbon content in the soils indicates that seagrass beds have
extremely high carbon storage potential, even in nutrient-limited areas with
low biomass or productivity.
Introduction
Increases in anthropogenic nutrient supply can alter coastal intertidal and
subtidal plant communities by increasing aboveground biomass, lowering
belowground biomass, or both (Deegan et al., 2012; Darby and Turner, 2008;
Herbert and Fourqurean, 2009; Turner et al., 2009). Such changes in plant
community structure are closely linked to the carbon storage potential of
vegetated coastal ecosystems – a topic of key interest in emerging carbon
markets (Russell et al., 2013; Couto et al., 2013; Alongi, 2014). Coastal
ecosystems provide valuable “blue carbon” sequestration capacity, and may
partially mitigate for or offset future climate change (Fourqurean et al.,
2012a; Saintilan et al., 2013). However, plant biomass is a relatively
labile carbon storage compartment – higher CO2 concentrations may
increase carbon storage in mangroves (Alongi, 2014) and seagrasses (Russell
et al., 2013; Campbell and Fourqurean, 2013), but chronic nutrient
enrichment may decrease it (Schmidt et al., 2012; Morris and Bradley, 1999).
Therefore, recent attention has turned to the longer-term carbon storage
compartment in the soil (Saintilan et al., 2013; Callaway et al., 2012).
Soil carbon is a large component of carbon storage in many coastal habitats
(Donato et al., 2011; Chmura et al., 2003; Duarte et al., 2005; Mcleod et
al., 2011; Armitage et al., 2011; Fourqurean et al., 2012a). The magnitude
of soil carbon storage is linked to the mineral and physical characters of
the soil (Rasmussen et al., 2007), with high carbon storage in soils with
more clay (Schimel et al., 1994). Microbial communities are equally but
inversely influential, with microbial decomposition and respiration
generally causing net efflux of carbon from the soils in a process known as
microbial priming (Schimel et al., 1994; Carney et al., 2007). The amount of
organic carbon in the soil can be positively linked to aboveground and
belowground plant productivity (Kirwan and Mudd, 2012). Seagrasses are
highly productive, and have a particularly large storage capacity, relative
to area (Fourqurean et al., 2012a). However, seagrass productivity is
sensitive to nutrient (e.g., nitrogen or phosphorus) input, often decreasing
substantially as a result of light limitation during macro- or microalgal
blooms (Hauxwell et al., 2001; Schmidt et al., 2012; Burkholder et al.,
2007). Therefore, near-term and long-term nutrient input may alter soil
carbon storage potential in seagrass beds.
The quantity of carbon stored in coastal habitats is the net balance between
inputs and losses. In nutrient-limited environments, nutrient addition
increases primary productivity and biomass of plants, thereby increasing the
rate of organic matter production, increasing trapping of allochthonous
carbon, and preventing erosion of deposited carbon (Hemminga et al., 1991;
Madsen et al., 2001; Gacia et al., 2002). Conversely, nutrients can
stimulate microbial activity; this microbial priming can mineralize an
otherwise recalcitrant pool of soil organic carbon (Carney et al., 2007;
Fontaine et al., 2003). The net effect is likely to be context-dependent;
the degree of nutrient limitation varies between sites and regions (De Boer,
2007), suggesting that the extent to which nutrients accelerate carbon loss
may vary among sites.
Patterns of nutrient input to and availability in coastal systems can be
driven by long-term, abiotic site conditions such as soil type or hydrology
(Duarte, 1995; Fourqurean and Zieman, 2002; Short, 1987). Frequently, these
mechanisms of nutrient supply and limitation are disrupted by near-term
anthropogenic inputs (Orem et al., 1999; Tomasko et al., 2005). Carbon
sequestration in the soil generally occurs on longer timescales (Callaway et
al., 2012; Hansen and Nestlerode, 2014), though stored carbon can be lost
quickly if vegetation or soils are disturbed by natural or anthropogenic
impacts (DeLaune and White, 2012), particularly at large spatial scales
(Macreadie et al., 2014). We evaluated the influence of long-term and
near-term nutrient history on aboveground and belowground carbon accumulation
in seagrass beds, using a nutrient enrichment experiment embedded within a
naturally occurring, long-term gradient of nutrient availability within
Florida Bay. In this system, P availability severely limits primary
production in much of the eastern Bay (Fourqurean et al., 1992), and N limits
some pelagic primary producers in the western Bay (Tomas et al., 1999). Our
objectives were to (1) evaluate the effects of near-term nutrient addition on
carbon storage in seagrass beds, and (2) determine if there was a
relationship between soil carbon and seagrass nutrient limitation, as
indicated by leaf nitrogen : phosphorus (N : P) ratios. In the P-limited
Florida Bay ecosystem, low N : P ratios indicate higher availability of the
limiting nutrient, P, and less severe long-term phosphorus limitation.
Methods
Our experimental design evaluated the near-term effects of nitrogen (N) and
phosphorus (P) enrichment on above- and belowground carbon storage across a
P-availability gradient. We used a three-way ANOVA design, where the factors
were P addition, N addition, and site (Armitage et al., 2011). In
September 2002 we established six study sites (all depths < 2 m)
within Everglades National Park in Florida Bay (Fig. 1). Most sites were
dominated by Thalassia testudinum; Halodule wrightii and
Syringodium filiforme were found at some sites, particularly the
westernmost site, Sprigger Bank (Fig. 1). The three eastern sites (Duck,
South Nest, Bob Allen) occurred in an area of severe P limitation (Armitage
et al., 2005; Fourqurean and Zieman, 2002). Two middle sites (Rabbit Key,
Nine Mile Bank) occurred in a region of low to intermediate P limitation
(Fourqurean and Zieman, 2002), and the westernmost site (Sprigger Bank) was
located in a region that had a balanced N and P supply (Armitage et al.,
2005). At each site we established a grid of 24 0.25-m2 study plots
spaced 1 meter apart. We randomly assigned treatments (control, nitrogen
only [N], phosphorus only [P], both nitrogen and phosphorus [NP]) to six
plots per site; fertilizer was added bimonthly from September 2002 through
April 2006; loading rates and application protocols are described in Armitage
et al. (2011).
Map of Florida Bay and the study sites.
In February 2004, soil cores (1 cm diameter, 5 cm deep) were collected from
each plot, dried at 60 ∘C, and homogenized for carbon analyses. A
separate set of cores (volume 5 mL each) was collected and weighed wet and
dry in order to calculate bulk density as grams of dry soil per liter.
In April 2006, we used a circular core (15 cm diameter, 15 cm deep) to
subsample seagrass biomass in each plot. Seagrasses were separated by
species, and tissue was divided into aboveground (photosynthetic) and
belowground tissue (rhizomes + roots + other non-photosynthetic
tissue). Epiphytes were removed by gently scraping seagrass leaves with a
razor blade. Cleaned seagrass tissues were dried at 60 ∘C and
weighed to determine biomass. Biomass results were reported by Armitage et
al. (2011), and were used here to calculate seagrass carbon stores in g
C m-2.
We measured the organic carbon (C) content of the soils and C, N, and P
content of above- and belowground seagrass tissue. Carbon and N contents were
determined using a CHN analyzer (Fisons NA1500), which reports nutrients as a
percent of dry weight. We used seagrass biomass (g m-2) and C content
to calculate aboveground and belowground seagrass carbon stocks in g C
m-2. Stocks for each species were summed to calculate total seagrass
carbon stocks in each plot. We applied the method described in Fourqurean et
al. (2012b) to assess the organic carbon (OC) content of our carbonate soils.
Briefly, total C content of the dry soil and of the residue remaining after
ignition at 500 ∘C for 4 hours was measured using a CHN elemental
analyzer; % OC was calculated as % TCdry-(% Cash× (dry weight of soil/dry weight of residue)).
This technique has been found to work well in the carbonate soils of Florida
Bay (Fourqurean et al., 2012b). Soil organic carbon content was calculated
from the % OC and the bulk density, and was reported as g C m-2 in
the top 15 cm of the soil. P contents were determined by a dry-oxidation,
acid hydrolysis extraction followed by a colorimetric analysis of phosphate
concentration of the extract (Fourqurean et al., 1992). Molar N : P ratios
were calculated for aboveground tissue of the most common seagrass species,
Thalassia testudinum.
The effect of near-term nutrient enrichment on carbon stores in aboveground
seagrass tissue, belowground seagrass tissue, and soils were analyzed with
three-way fixed factor ANOVA (P addition, N addition, and site) following
verification of homoscedasticity with Levene's test. Data were square root
transformed if necessary to conform to the assumptions of ANOVA.
To assess the influence of long-term nutrient history (as estimated by leaf
N : P in control plots) on soil carbon content, we used curve fit
regression analyses to identify the best fit relationships. Soil organic
carbon content (% or g m-2) from control plots were the dependent
variables in separate analyses, and Thalassia leaf N : P was the
predictor variable. We focused on Thalassia tissue because it was
the most common species and occurred in most study plots. Thalassia
was absent from the westernmost site, Sprigger Bank, so that site was
excluded from this analysis. In order to determine if soil carbon stock was
linked to seagrass productivity, we repeated this analysis with aboveground
and belowground seagrass carbon stores as the predictor variables. In the
curve fit analyses, we fitted regression models of increasing complexity to
each set of dependent and predictor variables, and accepted the model where
the predictive power (R2 value) was higher than simpler models, but
where that predictive power did not increase at the next step in model
complexity.
Results
The total carbon stock in aboveground seagrass tissue, which is a function of
seagrass biomass, was 3 to 10× higher in P-addition treatments, but
only at the three most P-limited sites in eastern Florida Bay
(Site × P p < 0.001; Table 1; Fig. 2a). The aboveground
carbon store was 10–30 % larger in many of the N addition plots
(Fig. 2a). Although there was no significant site × N interaction
(Table 1), the positive effects of N addition on the size of the aboveground
carbon store appeared to be strongest at the three western sites that were
not as severely P-limited (Fig. 2a).
Results of 3-way ANOVA of site, nitrogen (N), and phosphorus (P)
addition on the carbon stock in aboveground seagrass tissue.
(a) Aboveground and (b) belowground seagrass
carbon stocks at six sites in response to nitrogen (N) and phosphorus (P)
addition. Sites are displayed along a naturally occurring P-availability
gradient from low P availability in the east to high P availability in the
west.
As with aboveground seagrass tissue carbon, belowground seagrass tissue
carbon, a function of belowground biomass, also varied with site and P
addition (Site × P p < 0.001; Table 2), but the
site-specific responses were variable. Phosphorus addition increased
belowground seagrass carbon by 50–100 %, but only at one of the severely
P-limited sites (Bob Allen Keys; Fig. 2b). The belowground seagrass carbon
store was up to 30 % smaller in P-addition plots at two sites with more
moderate P limitation, Rabbit Key Basin and Nine Mile Bank (Fig. 2b). There
was no effect of N addition on belowground seagrass tissue carbon.
Results of 3-way ANOVA of site, nitrogen (N), and phosphorus (P)
addition on the carbon stock in belowground seagrass tissue.
Soil organic carbon content, expressed in g m-2, varied with site, N-,
and P-addition treatments (Table 3), but there were no consistent treatment
responses across sites. Differences among sites were not linked to long-term
nutrient history; the eastern-most and western-most sites had similar soil
organic carbon content. The effects of N and P addition on soil organic
carbon were generally small and variable, yielding a significant three-way
interaction term (Table 3; Fig. 3a). However, when expressed as a percent of
dry weight, soil organic carbon content was about 10 % lower in P
addition plots at some sites (Site × P p=0.011; Table 4),
especially the two sites with more moderate P limitation, Rabbit Key Basin
and Nine Mile Bank (Fig. 3b). A similar response occurred at the easternmost
site, Duck Key (Fig. 3b).
Results of 3-way ANOVA of site, nitrogen (N), and phosphorus (P)
addition on total soil organic carbon content (g m-2).
Soil organic carbon stocks, reported in (a) g m-2
and (b) percent at six sites in response to nitrogen (N) and
phosphorus (P) addition. Sites are displayed along a naturally occurring
P-availability gradient from low P availability in the east to high P
availability in the west.
Curve fit analysis with Thalassia leaf N : P ratio as the
predictor variable identified logarithmic regression as the best fit for both
measures of soil organic carbon content. Soil carbon content (in g m-2)
was significantly predicted by Thalassia leaf N : P (p= 0.009,
R2=0.243; Fig. 4a). Soil percent carbon content was also significantly
predicted by Thalassia leaf N : P (p < 0.001, R2=0.593). Soil percent carbon was markedly lower in the three eastern,
phosphorus-limited sites than in the western sites (Fig. 4b). There appeared
to be a threshold in the seagrass leaf N : P and soil carbon relationships:
when seagrass leaf N : P exceeded 75:1, there was less than 3 %
organic carbon in the sediment (Fig. 4b).
Results of 3-way ANOVA of site, nitrogen (N), and phosphorus (P)
addition on percent organic carbon in the soil.
Logarithmic relationship between Thalassia testudinum leaf
N : P ratio and soil carbon stock in control plots, reported in
(a) g m-2 and (b) percent. Sites are listed in the
legend in order from east (most P limited) to west (least P limited).
Curve fit analysis with Thalassia above- and belowground carbon
stocks as the predictor variables identified close relationships with both
measures of soil organic carbon content. Soil carbon content (in g m-2)
was significantly predicted by Thalassia aboveground carbon stock
(linear, p= 0.008, R2=0.242; Fig. 5a). Soil percent carbon
content was also significantly predicted by Thalassia aboveground
carbon stock (linear, p < 0.001, R2=0.716; Fig. 5b). Soil
carbon content (in g m-2) was significantly predicted by
Thalassia belowground carbon stock (linear, p < 0.001,
R2=0.419; Fig. 6a). Soil percent carbon content was also significantly
predicted by Thalassia belowground carbon stock (logarithmic,
p < 0.001, R2=0.791; Fig. 6b). There was an apparent
threshold in the seagrass belowground carbon and soil carbon relationships:
when seagrass belowground carbon stock was less than 100 g m-2, there
was less than 3 % organic carbon in the sediment (Fig. 6b).
Linear relationship between Thalassia testudinum
aboveground carbon stock and soil carbon stock in control plots, reported in
(a) g m-2 and (b) percent. Sites are listed in the
legend in order from east (most P limited) to west (least P limited).
Relationship between Thalassia testudinum belowground
carbon stock and soil carbon stock in control plots, reported in
(a) g m-2 (linear) and (b) percent (logarithmic).
Sites are listed in the legend in order from east (most P limited) to west
(least P limited).
Discussion
Soil carbon in Florida Bay seagrass beds was closely related to belowground
seagrass carbon stock and to landscape-scale nutrient limitation patterns.
Both of these relationships functioned on large temporal and spatial scales,
and near-term nutrient enrichment had a relatively small effect on soil
carbon. Thalassia leaf N : P is an accurate indicator of long-term
nutrient history (Fourqurean et al., 1992), and it was closely related to
soil % carbon, and, to a lesser degree, absolute soil carbon stock.
Patterns of nutrient limitation at this spatial scale are linked to
landscape-scale biomass and the rate of organic matter production (Herbert
and Fourqurean, 2009; Armitage et al., 2005). In more productive seagrass
beds, higher biomass increases trapping of allochthonous carbon, and prevents
the erosion of deposited carbon (Hemminga et al., 1991; Madsen et al., 2001;
Gacia et al., 2002), further augmenting soil carbon storage. Further, since a
substantial fraction of seagrass primary production is released from roots
and rhizomes as dissolved organic carbon (DOC) (Kaldy et al., 2006), the
supply of labile DOC to the sediments will be higher in dense seagrass
meadows with greater belowground biomass, relative to sparser seagrass beds.
This DOC supply could augment the % OC in soils underlying dense seagrass
meadows, or could act as a primer for the decomposition of refractory organic
compounds.
Soil characteristics such as grain size and mineral composition are
important influences on carbon storage and limiting nutrient
bioavailability, often shaping the long-term nutrient history of a site
(McGlathery et al., 1994; Schimel et al., 1994; Rasmussen et al., 2007).
There is generally greater net adsorption of organic matter onto finer
grained soils with higher surface areas (Mayer, 1994). The low shear stress
within seagrass beds is likely to augment the settlement and retention of
these small particles. In seagrass beds with higher biomass, the
depositional environment will facilitate the trapping of fine sediment,
creating a feedback that further increases the C content of the soils. In
fact, the physical effect of increased biomass on C deposition may be
similar in magnitude to the increased C supply in higher productivity beds.
In addition, phosphorus readily binds to carbonate sediments such as those
in Florida Bay (Short et al., 1985; McGlathery et al., 1994), and P is
efficiently retained in the sediments for decades following near-term P
enrichment experiments (Herbert and Fourqurean, 2008). Therefore, the
effects of near-term enrichment may persist long after a fertilization event
(Fourqurean et al., 1995). The carbonate sediments in our study system
likely played an important role in controlling seagrass productivity and
subsequent belowground input to the soil carbon stock.
Soil carbon content is often closely linked to microbial priming activity,
where higher microbial respiration and decomposition rates will accelerate
carbon efflux from the soil (Waldrop et al., 2004; Kirwan and Blum, 2011;
Cleveland and Townsend, 2006). In many ecosystems, priming is augmented in
response to near-term nutrient enrichment, leading to a net loss of soil
carbon (Schimel et al., 1994; Carney et al., 2007; Sayer et al., 2011). In
our study, fertilization had relatively small effects on soil carbon stores.
There was a small (∼ 10 %) decrease in absolute soil carbon content
in response to phosphorus addition, but only at three of the sites – one in
the eastern Bay, and two in the nutrient-replete western Bay. Priming effects
on soil carbon are complex, and are not simply based on nutrient availability
– competition among microorganisms also plays an important role (Fontaine et
al., 2003). Alternatively, there may have been an offset between carbon gains
from higher belowground productivity (Armitage et al., 2011) and carbon
losses due to microbial priming, resulting in little to no net change in
carbon storage.
There was a relatively small response of soil carbon to our near-term,
small-scale nutrient enrichment treatments. Although there was an increase
in above- and belowground biomass following phosphorus enrichment at the
eastern bay sites (Armitage et al., 2011), the biomass accumulation was not
sufficient to affect soil carbon at the timescale of our experiments. In
the western bay, there was greater ambient phosphorus availability, and
therefore more benthic productivity at large spatial scales (Armitage et
al., 2011). In the eastern bay, only small plots received fertilizer and
therefore had high biomass; surrounding areas had very low biomass. The
deposition and retention of organic matter into seagrass beds is influenced
by surrounding production (Gacia et al., 2002), suggesting that the
effective retention of autochthonous or allochthonous organic carbon
requires larger areas of high biomass. In restored seagrass beds, it may
take more than 10 years for soil carbon accumulation rates to reach levels
comparable to established seagrass beds (Greiner et al., 2013). Our eastern,
phosphorus-limited sites had little biomass at the start of the study
(Armitage et al., 2005), comparable to a newly initiated restoration
project. Therefore, it is likely that enrichment would have to continue for
many years before responses in soil carbon stores could be detected.
Although added phosphorus can be retained for decades in this system
(Herbert and Fourqurean, 2008), the spatial scale of our enrichment
treatments was small, relative to the landscape, and had low potential to
trap allochthonous organic carbon (Armitage et al., 2011). Therefore, soil
carbon sequestration and plant biomass responses to nutrient enrichment
appear to act on very different spatial and temporal scales.
An important predictor of soil organic carbon content in our study was
seagrass biomass, particularly belowground biomass. The link between plant
productivity and soil carbon storage is well known in terrestrial and marine
ecosystems (e.g., De Deyn et al., 2008; Mcleod et al., 2011; Kirwan and
Mudd, 2012). Soil carbon storage potential can be particularly high in
seagrass beds, relative to biomass and area (Fourqurean et al., 2012a).
However, soil carbon content is not consistently related to seagrass biomass
(Campbell et al., 2015), suggesting that seagrass productivity is not the
sole predictor of soil carbon stores. In regions where soil carbon storage
is not directly related to seagrass productivity, carbon capture is
augmented by the entrapment of a substantial amount of particulate carbon
(Mcleod et al., 2011) and slow decomposition rates in the soil (Duarte et
al., 2013).
Plant productivity is linked to long-term nutrient history (e.g., Day et al.,
2006; Herbert and Fourqurean, 2009). Accordingly, we expected that plant
productivity, and corresponding carbon storage, would be higher in our study
sites with less severe phosphorus limitation. This prediction was borne out
to some degree – the western sites had lower Thalassia leaf N : P
ratios and higher soil carbon, but there was a nonlinear relationship between
seagrass leaf N : P and soil carbon. When seagrass leaf N : P exceeded an
approximate threshold of 75:1, suggesting severe phosphorus limitation
(Armitage et al., 2005), there was less than 3 % organic carbon in the
sediment. Despite the marked difference in soil carbon between
phosphorus-limited and phosphorus-replete areas of Florida Bay, all areas of
the Bay had relatively high soil carbon stocks. The severely
phosphorus-limited eastern Bay had soil carbon content near the global median
of 1.8 % soil organic carbon content (Fourqurean et al., 2012a). Soil
carbon content in the nutrient-replete western Bay exceeded that of
productive seagrass beds in many other coastal regions (Campbell et al.,
2015; Duarte et al., 2005; Kennedy et al., 2010; Lavery et al., 2013). The
relatively high carbon content in the soils indicates that seagrass beds have
extremely high carbon storage potential, even in nutrient-limited areas with
low productivity.
Conclusions
Near-term fertilization had a relatively minor impact on soil C stores
despite large increases in living biomass. Long-term nutrient history, which
controls productivity in this landscape, was linked to both biomass and soil
C stocks. Higher biomass should result in more efficient trapping of fine
particles and organic matter in the sediments, suggesting that there could be
a physical effect of increased biomass that rivals the influence of increased
productivity. Therefore, long-term changes in nutrient supply to oligotrophic
coastal ecosystems could increase C storage, provided that enrichment does
not cause plankton or algal blooms that lead to the loss of seagrasses.
Data availability
All data used in this study are included in this manuscript and associated
in the Supplement.
The Supplement related to this article is available online at doi:10.5194/bg-13-313-2016-supplement.
A. R. Armitage and J. W. Fourqurean designed the experiments and
A. R. Armitage carried them out and analyzed the data. A. R. Armitage
prepared the manuscript with contributions from J. W. Fourqurean.
Acknowledgements
This research was funded by a grant from the Everglades National Park (ENP)
under cooperative agreement 1443CA528001022 and in collaboration with the
Florida Coastal Everglades Long-Term Ecological Research Program under
National Science Foundation Grant Nos. DEB-9910514 and DBI-0620409. Doug
Morrison and Bill Perry facilitated permit issuance and use of ENP
facilities. We are grateful to the many people who devoted field and
laboratory time to this project. Pursell Technologies Inc. and IMC Global
generously donated the nitrogen and phosphorus fertilizers, respectively,
for this study. The open access publishing fees for this article have been
covered by the Texas A&M University Online Access to Knowledge (OAK)
Fund, supported by the University Libraries and the Office of the Vice
President for Research. This is contribution number 749 from the Southeast
Environmental Research Center at FIU.
Edited by: E. Marañón
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