Carbon dioxide exchange between the atmosphere and forested subtropical
wetlands is largely unknown. Here we report a first step in characterizing
this atmospheric–ecosystem carbon (C) exchange, for cypress strands and pine
forests in the Greater Everglades of Florida as measured with eddy
covariance methods at three locations (Cypress Swamp, Dwarf Cypress and Pine
Upland) for 2 years. Links between water and C cycles are also examined at
these three sites, as are methane emission measured only at the Dwarf Cypress
site. Each forested wetland showed net C uptake from the atmosphere both
monthly and annually, as indicated by the net ecosystem exchange (NEE) of carbon
dioxide (CO
On global scales, wetlands are generally considered sinks for atmospheric
carbon dioxide (Troxler et al., 2013; Bridgham et al., 2006) and natural
sources for methane emission (Whalen, 2005; Sjogersten et al., 2014). Wetlands
in southern Florida's Greater Everglades (
In addition to the insight provided on the role of subtropical forested
wetlands in the global carbon cycle, this research is expected to be useful
for determining consequences of land-use changes in the Everglades region.
Canal building and drainage projects in south Florida have reduced the
original extent of the Everglades (Parker et al., 1955), decreased peat
accretion rates and total carbon stocks, and reduced ecosystem services.
Hohner and Dreschel (2015), for example, estimate that the Greater Everglades has
less than 24 % of its original peat volume and 19 % of its original carbon.
In response, state and federal governments are planning and executing
complex projects to restore the Everglade's wetlands (
Restoring ecosystems will affect water, energy and C cycles, as plants and soil processes adjust to changing water levels, salinities, nutrient loads and fire regimes. For example, Jimenez et al. (2012) and Schedlbauer et al. (2010) indicate that additional deliveries of water into peat and marl sawgrass wetlands may diminish C accumulation within these wetlands. Eddy-covariance-derived estimates of net ecosystem productivity declined with increasing inundation during the wet season (Jimenez et al., 2012; Schedlbauer et al., 2010). These results were partially attributed to the amount of vegetation that, due to flooding, could not directly exchange carbon dioxide with the atmosphere. The opposite trend was observed in a tidally influenced mangrove forest in the Everglades National Park. Lowered salinities, resulting from increased freshwater flow, resulted in increased daily PAR-use efficiency (i.e., the ratio of gross ecosystem productivity to photosynthetically active irradiance (PAR; Barr et al., 2010, 2012)). Also, ecosystem respiration losses were lower during periods of inundation (Barr et al., 2010, 2012), which increased net C uptake over the mangrove forest. These studies provide insights into water and C cycling over coastal sawgrass wetlands and mangrove forests. C cycling over other subtropical wetlands, such as cypress strands and pine forests, is largely unstudied (Sjogersten et al., 2014).
The primary goal of this paper is to quantify the magnitude and controls of C exchange within cypress- and pine-forested wetlands. These wetland communities are defined by McPherson (1973), Duever et al. (1986) and Duever (2002). Quantities of interest include the net atmospheric–ecosystem C exchange (NEE), ecosystem respiration (RE), gross ecosystem exchange (GEE) and methane emissions. Latent heat flux (LE) and evapotranspiration (ET) are also quantified so that links between water and C cycles can be quantitatively studied. We address several specific objectives on daily, monthly and annual timescales, including (1) the magnitude of cypress- (tall and dwarf) and pine-forested wetlands as net atmospheric C sources or sinks, (2) site differences in water and C exchange metrics (i.e., NEE, GEE, RE and surface energy fluxes), and (3) the magnitude of methane emission over a dwarf cypress wetland. Results from this study are expected to help define and predict responses of subtropical forested wetlands to regional (e.g., freshwater discharge) and global (e.g., air temperature) environmental change.
The study area is the Big Cypress National Preserve (BCNP) in southern Florida (Fig. 1). A variety of subtropical forested and non-forested wetland ecosystems are present in BCNP, including Pine Upland, Wet Prairie, Marsh, Hardwood Hammocks, Cypress Swamps, Dwarf Cypress and Mangrove Forests as formally characterized by McPherson (1973) and Duever et al. (1986, 2002). The distribution of ecosystems and plant communities in the BCNP is controlled by topography, hydrology, fire regimes and soil conditions (Duever et al., 1986). Marsh, Cypress Swamp, and Mangrove Forests typically occupy low elevations (< 2.5 m national geodetic vertical datum, NGVD-29), Wet Prairie occupies middle elevations (3 to 4 m NGVD-29), and Pine Uplands and Hardwood Hammocks occupy high elevations (> 4 m NGVD-29). These wetlands provide floodwater protection, hurricane buffering, substrate stabilization, sediment trapping, water filtration and other ecosystem services for urban areas and coastal estuaries.
Water and C fluxes were determined over Pine Upland, Cypress Swamp and Dwarf
Cypress ecosystems (Fig. 1, Table 1) from December 2012 to November 2014
(Shoemaker et al., 2015d, e, f). The Pine Upland site (Fig. 2, Table 1),
is classified as a mixed lowland pine site and is located in an extensive
open-canopy pine forest with numerous small- to medium-sized cypress domes.
The canopy is dominated by slash pine (
The Cypress Swamp site (Fig. 2, Table 1) is classified as a swamp forest
(Duever et al., 1986) and supports a tall, dense cypress forest with a
subcanopy of mixed hardwoods (Fig. 2). Plant varieties include bald
cypress (
The Dwarf Cypress site is classified as scrub cypress and is dominated by
cypress,
Location of the study area and vegetation communities, modified from Duever (2002).
Panoramic photos of the
Site locations, tower heights and summary of vegetation.
A mass balance equation can be used to conceptualize C fluxes. Net ecosystem
C balance (NECB) is the amount of C accumulating in the ecosystem, given in units
of mass per area–time (Chapin et al., 2006; Troxler et al., 2013). NECB can
be partly approximated using eddy covariance methods by measuring (1) the
net vertical (one-dimensional) exchange of carbon dioxide (NEE) across the
ecosystem–atmosphere interface, (2) the net lateral flux (
The eddy covariance method (Dyer, 1961; Tanner and Greene, 1989) is a one-dimensional (vertical) approach for measuring the exchange of gases within the atmospheric surface layer (Campbell and Norman, 1998). Key instrumentation (Table 2) includes sonic anemometers that rapidly (10 Hz) measure wind velocity and gas analyzers that rapidly measure gas concentrations (Table 2) in the atmosphere. The covariance between vertical wind velocities and gas concentrations determines the net exchange of gases between the ecosystem and the atmosphere. Additional instrumentation (Table 2) was installed at each site to measure net radiation, soil-heat flux, soil temperatures, air temperature and relative humidity, and the distance of water above or below land surface (using pressure transducers). Pressure transducers were placed at the bottom of groundwater wells to measure the distance of water above and below land surface. Pressure transducers were corrected monthly for instrumentation drift using manual depth-to-water measurements from the top of the well casings. The manual depth-to-water measurements allowed the precise calibration of continuous water distance above or below land surface. Monthly site visits were made to download data, perform sensor inspections and complete other site maintenance. All instrumentation was visually inspected, leveled, cleaned or replaced as necessary.
Raw, 10 Hz, vertical wind speed, temperature and gas concentration data
were processed to half-hourly fluxes using EddyPro software (version 4.0.0)
following advanced protocols that included random uncertainty estimates
(Finkelstein and Sims, 2001), spiking filters, double coordinate rotations,
blocked-average detrending, statistical filters, air density and oxygen
corrections (Tanner and Thurtell, 1969; Baldocchi et al., 1988; Webb et
al., 1980; Tanner et al., 1993), and high-pass filtering. Processed data
yielded half-hourly mean values of NEE, methane, and sensible and latent heat
fluxes that were filtered to remove periods with unrealistic fluxes
(Cypress Swamp – latent heat fluxes > 800 and <
Following EddyPro processing, local despike and friction velocity filters
were applied to the gas fluxes (Shoemaker et al., 2015d, e, f). The local
despike filter removed half-hour fluxes that fell outside 3 standard
deviations of the fluxes within a moving 7-day window. Friction velocity is
an indicator of time periods when turbulent wind conditions are well
developed. Eddy covariance methods are appropriate for turbulent wind
conditions. The
Instrumentation installed at the Dwarf Cypress, Cypress Swamp and Pine Upland flux stations.
At the Pine Upland site, NEE contamination was possible due to fossil fuel
combustion by generators and trucks supporting oil-drilling activities
adjacent to the eddy covariance tower. Thus, all carbon fluxes were removed
at Pine Upland when the wind direction was from the east of the tower (15 to
130
Missing 30 min fluxes (NEE, LE, H) were gap-filled using a lookup table
approach (Table 3) documented in Reichstein et al. (2005). The lookup table
replaces missing fluxes with available fluxes collected during similar
meteorological conditions (net radiation within 50 W m
Positive NEE during the night was assumed to represent ecosystem respiration
(RE). RE was weakly correlated with quantities such as air temperature
(
Methane emissions (
Seasonally, missing daily
Gap-filling results for fluxes based on the lookup table approach by Reichstein et al. (2005).
Daily NEE, RE and
The subtropics of south Florida are characterized by distinct wet and dry seasons driven by changes in solar insolation, air temperature, humidity and rainfall. Rainfall and photosynthesis are greatest in the hot and humid spring and summer months from about May to October. The end of October generally marks the end of the wet season (and hurricane season). Wetland water levels and surface energy fluxes are tightly coupled to seasonality in heat and humidity. Cold fronts are especially remarkable within surface energy budgets, as dry cold air passes over relatively warm soil and surface water, creating large variations in both stored-heat energy and turbulent fluxes of heat and water vapor (Shoemaker et al., 2011).
Observed and computed mean daily molar methane (CH
Mean daily temperature and surface energy fluxes. Dates are given in the format month/day/year.
During this study, air temperatures at all three sites (Fig. 4a–c) were
seasonally lowest (ranging from 15 to 25
Seasonality was observed in water levels at each site (Fig. 4a, b and c)
in response to rainfall duration and intensity. Water levels were lower in
the winter and early spring due to reduced rainfall at the end of the dry
season (i.e., November to May). Water levels rose in response to rainfall at
the end of April 2013 and May 2014, reaching
Surface energy fluxes reflected the seasonality in air temperature and
rainfall (Fig. 4a, b, c). Mean daily net radiation ranged from about 50 to
over 200 W m
Monthly and annual C and methane fluxes.
All three sites were generally sinks of atmospheric carbon dioxide
(CO
The Moderate-resolution Imaging Spectroradiometer (MODIS) enhanced
vegetation index (EVI) served as a useful qualitative surrogate for seasonal
terrestrial photosynthetic activity and canopy structural variations (Fig. 5), as reported for some other studies (Huete et al., 2002). EVI over a tall
mangrove forest, for example, varied seasonally between 0.35 and 0.55 and
decreased to
Seasonal patterns in NEE and GEE were consistent with changes in EVI (Fig. 5a, b, c), most notably at the Cypress Swamp site. Increases in EVI from 0.25 to 0.35 corresponded with growth of cypress leaves on relatively tall (18 to 21 m) and densely spaced cypress trees (Fig. 2) beginning in about March to April. Cypress leaves discontinued growing in August to September and turned brown in October, eventually falling into the sawgrass and hardwood understory. This lack of photosynthetic activity corresponded with changes in EVI of 0.4 to 0.2 in the summer and in the winter (Fig. 5b), respectively, of 2013 and 2014 at the Cypress Swamp flux station.
Daily and monthly C fluxes, stage and EVI at the
Gross atmosphere–ecosystem C exchange (GEE) provides a first approximation
of gross ecosystem productivity (GEP) or the accumulation of C in the plant
canopy. Growth and senescence of cypress leaves was most evident in monthly
GEE (Fig. 5, Table 4) at the Cypress Swamp site, where rates increased
from about 100 g C m
A key water and ecosystem management issue in south Florida, and globally,
is the preservation of organic soils within wetlands (Hohner and Dreschel,
2015) to (1) support ecosystem services and (2) maintain or grow
topography. Growing topography via C accumulation in these coastal forested
wetlands could partly offset sea-level rise. Inundation suppressed
respiration most remarkably at Cypress Swamp and Pine Upland (Fig. 5a, b).
RE doubled from about 60 to 120 g C m
Relationships between net ecosystem C exchange (NEE) and latent heat flux
(LE) reflect an important link between water and C cycles (Fig. 6), that
is, photosynthesis that releases water (transpiration) while storing C.
Relations between latent heat flux and net ecosystem exchange.
Coupling between water and C cycles was examined via water-use efficiencies
(WUEs) (Table 5) computed as the ratio of annual NEE to ET. As such, WUEs are the
net mass or moles of C transferred to the ecosystem per millimeter or mole of water
vapor. Computing WUE with NEE accounts for the loss of C through
Methane is produced by anaerobic bacteria decomposing organic matter in the soil or in surface water. Methane can be oxidized during transport from the soil or surface water into the atmosphere. Transport to the atmosphere may occur through (1) roots and stems of vascular plants (Wang and Han, 2005; Morrissey et al., 1993; Kim and Verma, 1998), (2) ebullition as gas bubbles from anaerobic soils (Comas and Wright, 2012) and (3) diffusion through the soil and surface water (Van Huissteden et al., 2006; Christensen et al., 2003a, b). Methane emission is enhanced as anaerobic bacteria become more active at higher temperatures (Simpson et al., 1995).
At the Dwarf Cypress site, methane emission increased with increasing air temperature and water level in the summer months from June to September 2013 (Fig. 5c). In contrast, methane emission was suppressed from April to June 2014 due to dry conditions and perhaps the memory of dry conditions from July to September 2014. Anaerobic bacteria may take some time to reestablish following dry conditions. This reestablishment or “memory” of dry conditions would reduce methane emission despite warm conditions and flooding from July to September 2014.
Methane emission peaked at different times in the summer of 2013 compared to GEE at the Dwarf Cypress site (Fig. 5c). GEE peaked with photosynthesis in July 2013 whereas methane emission peaked in August 2013. This time lag indicates that the processes governing C exchange and methane emissions are quite different, with GEE controlled by the photosynthesis of cypress leaves and sawgrass, which grow vigorously from March to April and discontinue growth from August to September. In contrast, methane emission is driven by the anaerobic decomposition of organic matter with subsequent oxidation through the soil and surface water. Organic decomposition was enhanced in August 2013 by flooding and relatively warm air, soil and surface water.
ET, NEE and WUE at the flux stations.
Although methane emission is important in terms of global warming potential
(GWP), it appears to be immaterial in C budgets that alter or “grow” land
surface topography. C released from methane emission was relatively small
(averaging about 10 g C yr
A comparison of our results with NEE from selected previous studies
(Schedlbauer et al., 2010; Jimenez et al., 2012; Barr et al., 2010; Botkin et
al., 1970; Jones et al., 2014) reveals substantial spatial and temporal
heterogeneity in C uptake over geologic time and among different ecosystems
(Table 6). Subtropical forested wetlands exchange more C than temperate
forests (Botkin et al., 1970; Sjogersten et al., 2014). A study assessing C
exchange on a geologic timescale (Jones et al., 2014) also concluded that
long-term rates of C uptake in the Everglades are higher than in northern
latitudes and in some cases rival C uptake in tropical peatlands, such as
Indonesia. Mangrove ecosystems may serve as an upper limit for subtropical C
uptake, with an NEE of about
Sparse sawgrass wetlands in the Everglades, such as Taylor and Shark River
sloughs, are relatively minor atmospheric C sources or sinks, with NEE
ranging from
Atmospheric–ecosystem carbon dioxide exchange, methane emission and latent and sensible heat fluxes were estimated with eddy covariance methods for subtropical forested cypress and pine wetlands for 2 years. Seasonality in solar insolation, air temperature, plant physiological activity, rainfall and water levels created seasonality in C exchange rates and surface energy fluxes. Links between water and C fluxes were also revealed, such as photosynthetic water-use efficiencies.
Each forested wetland was an atmospheric C sink on monthly and annual timescales.
Atmospheric C uptake (NEE) was greatest at Cypress Swamp (
Respiration was enhanced when water levels dropped below land surface within these cypress- and pine-forested wetlands. Increases in respiration were likely due to heterotrophic soil respiration supplementing autotrophic respiration. These results highlight the importance of flooding and hydroperiod management for maintaining organic soils and peat accretion within subtropical forested wetlands, a key water and ecosystem management issue in south Florida and globally.
Links between water and C cycles were examined via (1) WUEs expressed as the ratio of annual NEE to ET and (2) correlations between NEE and LE. Computing WUE with NEE accounts for the loss of C through respiration. The Cypress Swamp and Pine Upland sites were most efficient at using water to store C, with WUE equal to about 1.0 g C per millimeter ET. About 0.5 g C was stored in the ecosystem per millimeter of ET at the Dwarf Cypress site. These results indicate that wetlands with more open-water surface are less efficient at using water to store C than forested wetlands. This pattern is likely to be true both regionally and perhaps globally, and thus, may have implications for the global C cycle.
Comparison of annual totals of NEE for different studies.
Correlations between NEE and LE reflected photosynthesis, which released water as transpiration while storing C. The strength of the NEE and LE correlation provided an indication of the relative magnitudes of transpiration and evaporation at each site. Transpiration was a large proportion of evapotranspiration at the Cypress Swamp and Pine Upland sites, as indicated by correlations of 0.34, 0.36 and 0.18 for the Cypress Swamp, Pine Upland and Dwarf Cypress sites, respectively. These results indicate that a redistribution of plant communities toward more open-water ecosystems could create less C uptake and greater evaporative losses.
Methane emission at Dwarf Cypress was considerable in terms of global
warming potential but immaterial in C budgets that build and maintain
land-surface topography. Approximately 14 g CH
This study was funded, in part, by the US Geological Survey (USGS) Greater
Everglades Priority Ecosystems Science (GEEES). Nick Aumen is acknowledged
for helpful conversations about the Everglades during project meetings and
fieldwork in BCNP. Michael J. Duever provided detailed vegetation
descriptions and guidance during site selection. Steve Krupa and Cynthia Gefvert from the South Florida Water Management District funded tower
construction. USGS peer reviews by Lisamarie Windham-Myers, Dave Sumner and
Kim Haag improved the quality of the manuscript. Biogeoscience peer reviews
by Ankur Desai and an anonymous referee also greatly improved the
manuscript. Any use of trade, firm or product names is for descriptive
purposes only and does not imply endorsement by the US Government. The
data used to create this manuscript is openly available to the public at