Leaching and microbial degradation of dissolved ... - Springer Link

Aquat Sci (2014) 76:595–609 DOI 10.1007/s00027-014-0357-4

Aquatic Sciences

RESEARCH ARTICLE

Leaching and microbial degradation of dissolved organic matter from salt marsh plants and seagrasses Xuchen Wang • Robert F. Chen • Jaye E. Cable • Jennifer Cherrier

Received: 27 January 2014 / Accepted: 23 June 2014 / Published online: 9 July 2014 Ó Springer Basel 2014

Abstract Dissolved organic matter (DOM) is outwelled from highly productive salt marshes, but its sources and fates are unclear. To examine common salt marsh plants as sources of coastal DOM, two dominant salt marsh vascular plants Spartina alterniflora and Juncus roemarianus, and two major coastal seagrasses Syringodium filiforme and Halodule wrightii, were collected from a Florida salt marsh and studied using laboratory incubation experiments. We investigated the leaching dynamics of dissolved organic carbon (DOC), total dissolved nitrogen (TDN), and chromophoric dissolved organic matter (CDOM) from these plants, in conjunction with our field investigations of the sources and outwelling of DOM from Florida salt marshes. The leaching of DOM and CDOM from the plants was a rapid process, and leaching rates were 65–288 lM/ g dry weight/day for DOC and 3.8–16 lM/g dry weight/ day for TDN from different plants in the bacteria-inhibited incubations. DOC was proportional to TDN in the leachates, but the quantity of C and N leached was dependent on

X. Wang (&) Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Ocean University of China, Qingdao 266100, China e-mail: [email protected] X. Wang R. F. Chen School for the Environment, University of Massachusetts at Boston, Boston, MA 02125, USA J. E. Cable Department of Marine Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA J. Cherrier School of the Environment, Florida A&M University, Tallahassee, FL 32307, USA

the species and growth stage of the plants. At the end of the 25-day experiments, 5.4–23 % and 10–45 % of solid phase C and N were released into DOC and TDN pools, respectively. Bacteria played an important role during the leaching process. The majority of DOC and TDN leached from marsh plants and seagrasses was labile and highly biodegradable with 56–90 % of the leached DOC and 44–72 % of the leached TDN being decomposed at the end of the experiments. The fluorescence measurements of CDOM indicate that organic matter leached from marsh plants and seagrasses contained mainly protein-like DOM which was degraded rapidly by bacteria. Our study suggests that leaching of DOM from salt marsh plants and seagrasses provide not only major sources of DOC, TDN, and CDOM that affect many biogeochemical processes, but also as important food sources to microbial communities in the marsh and adjacent coastal waters. Keywords Dissolved organic carbon Chromophoric dissolved organic matter Salt marsh Marsh plant Seagrass

Introduction Salt marshes and seagrass meadows are highly diverse and productive ecosystems widely distributed along coasts worldwide (Adam 1990; Hemminga and Duarte 2000). In the Gulf of Mexico, for example, about two-thirds of the 14,500 km2 of estuarine wetland along the coast are intertidal salt marshes. Salt marshes are typically characterized by dense vegetation including rushes, sedges, and grasses, and these vascular plants represent not only a large component of living biomass, but also the dominant primary producer in salt marshes (Nixon 1980; Pomeroy and

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Wiegert 1981; Marinucci 1982). For example, Spartina alterniflora, as the single dominant plant species, contributed over 81 % of the total primary production in the intertidal salt marshes along the East Coast of the United States (White et al. 1978; Pomeroy et al. 1981; Turner 1993). Similar to salt marsh plants, seagrass growing in the shallow coastal waters can often form extensive meadows with high production and biomass. Duarte and Chiscano (1999) estimated that on a global scale, production of seagrasses could contribute 1.13 % of the total marine primary production and that about 12 % of the total carbon storage in marine ecosystems was stored as living seagrass biomass. Hence, the high productivity and rapid turnover of salt marsh plants and seagrasses represent not only significant global carbon sinks (Duarte et al. 2010; Kennedy et al. 2010), but also major sources of organic carbon to coastal waters (Duarte et al. 2005). The ability to release dissolved organic carbon (DOC) while still acting as major carbon sequestration reservoirs underlies the important role that these coastal wetlands and seagrass meadows play in biogeochemical processes and the coastal carbon cycle. Export of DOC from salt marshes and seagrass beds to coastal waters has been considered an important link between these coastal ecosystems and the ocean (Penhale and Smith 1977; Pakulski 1986; Fry et al. 1992; Opsahl and Benner 1993; Hopkinson et al. 1998; Duarte et al. 2005). Previous studies have shown that DOC outwelling from southeastern US salt marshes alone could contribute an equal amount of DOC as river inputs to the continental shelf (Dame et al. 1991; Moran et al. 1991). Contribution of DOC from marshes and seagrass beds is largely through the leaching and decomposition of marsh plant and seagrass biomass. In the last decades, many studies have been conducted in both field and laboratory experiments to investigate the leaching and decomposition of salt marsh plants and seagrasses as potential sources of DOC and nutrients to coastal waters (Penhale and Smith 1977; Moran and Hodson 1990; Fry et al. 1992; Opsahl and Benner 1993; Turner 1993; Wang et al. 2007). Studies have shown that DOC production from decaying plant biomass was related to seasonal patterns of marsh and coastal metabolism and environmental factors (Valiela et al. 1985; Pakulski 1986; Turner 1993; Wang et al. 2007). Estimates for DOC production from aboveground biomass of S. alterniflora range from 0.5 to 17 mol C/m2/y (Gallagher et al. 1976; Pakulski 1986; Turner 1993). Turner (1993) found that when the marsh plant S. alterniflora was submerged in seawater, the release rate of DOC was 15 times higher than that of non-submerged plants. Compared to marsh plants, seagrasses have been found to decompose relatively rapidly in temperate systems (Newell et al. 1984; Harrison 1989; Peduzzi and Herndl 1991; Pedersen et al. 1999; Davis et al. 2006). Despite the understanding that a large

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source of DOC is produced from salt marsh plants and seagrasses, the chemical composition and bioavailability of DOC produced from different plant species have been less studied. There is limited knowledge on exactly how this DOC pool is recycled and its significance to biogeochemical processes in marsh and coastal waters. In addition to DOC, salt marsh plants are also major sources of chromophoric dissolved organic matter (CDOM) to estuarine and coastal waters (Filip and Alberts 1988; Coble 1996; Gardner et al. 2005; Wang et al. 2007; Huang and Chen 2009). In coastal waters, CDOM comprises a significant fraction of dissolved organic matter (DOM). Due to the importance of CDOM in affecting the optical properties of seawater and its role in photochemical and biochemical processing of DOC, CDOM has been studied extensively in recent years (Chen et al. 2004; Helms et al. 2008; Huang and Chen 2009; Osburn and Stedmon 2011). In the Plum Island salt marsh system in Massachusetts, USA, a study found that marsh plants, mainly S. alterniflora, contributed up to 90 % of the CDOM exported from the Parker River into Plum Island marsh estuary (Berry et al. 2002). In laboratory incubation experiments, Wang et al. (2007) measured that the CDOM leached from marsh grasses Spartina patens and Typha latifolia was proportional to the DOC produced. Additionally, CDOM produced from marsh plants was degraded more rapidly in oxic waters than in anoxic waters. Less attention has been focused on seagrasses, which could also be a CDOM source in coastal waters. The chemical composition of the CDOM produced from different salt marsh plants and seagrasses and the contribution of CDOM produced by salt marsh grasses to the coastal carbon cycle and microbial processing are poorly understood. In this paper, we present the results from laboratory leaching experiments using two dominant salt marsh plants and two seagrasses collected in a Florida salt marsh system. This study is part of a joint research project to investigate the sources and outwelling of DOM in the salt marsh system. In well-controlled laboratory incubation experiments, we quantitatively determine the leaching dynamics and characterize the DOC, total dissolved nitrogen (TDN), and CDOM leached from marsh plants and seagrasses. These results offer important insights into how salt marshes and other coastal wetlands will respond to climate change and the expected rise of sea levels over the next 50 years.

Materials and method Study site Snipe Creek salt marsh is located in the Florida Big Bend region (80 km south of Tallahassee; 30°04.314N;

Leaching and degradation of DOM in salt marshes

083°57.076W). The extensive salt marsh system is one of the largest (665 km2) and most pristine salt marshes of the US coast, extending from Apalachicola Bay to Cedar Key, FL, and accounts for about two-thirds of the marshes in northern Florida along the shoreline of the northeast Gulf of Mexico (Montague and Odum 1997). The marsh system has a small topographic slope (0.4 m/km), resulting in extensive shallow water across several 10 s of km in the coastal region. Two of the dominant halophytes that reside in the marshes are black needlerush, Juncus roemerianus, a C3 plant forming extensive monotypic halophyte stands within the middle-to-upper marshes, and smooth cordgrass, S. alterniflora, a C4 plant populated in the marsh’s low tidal regions along creek banks and around interior ponds (Touchette et al. 2009). In addition, the coastal region surrounding the Snipe Creek study area is characterized by a sea floor widely covered by the two dominant seagrass species, Syringodium filiforme and Halodule wrightii, forming an abundance of mixed seagrass beds. It is estimated that in the Florida Big Bend region alone, seagrass beds cover about 732 km2 of the coastline (Sargent et al. 1995). Due to the high abundance and productivity of both these marsh plants and seagrasses, it is expected that they will contribute significant amounts of both DOC and CDOM to the marsh tidal and inner shelf coastal waters. Sample collection Marsh plants, S. alterniflora and Juncus roemarianus, and seagrasses, S. filiforme and H. wrightii, were collected during November 20–27, 2010 and April 10–17, 2011 field campaigns. The two marsh plants were collected in November during their senescing stage and in April during their spring growing season to compare DOM release from these plants at different developmental stages and seasons. We collected the aboveground fraction of the plants, including stems and leaves. For the seagrasses, we collected fresh Syringodium in April 2011 during the growing stage and dying brown-colored H. wrightii in late November 2010 at the end of the growing season. After collection, samples were stored in clean plastic bags and kept fresh in a refrigerator. For the incubation experiments, relatively low DOC and CDOM seawater was collected from *1 km offshore of the marsh during the April 2011 trip. The water was filtered using 0.7 lm GF/F filters (precombusted at 500 °C for 5 h) to remove particles and transferred back to our laboratory on ice. Plant leaching experiments For leaching experiments, all plants and seagrasses were thoroughly washed with the filtered offshore seawater to remove any sediment. Two sets of leaching experiments

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were conducted: (1) bacteria-inhibited (poisoned) and (2) bacteria-active (non-poisoned), to quantify the chemical leaching process and determine the influence of bacterial activity on the leaching process. We only conducted one set of incubations for each treatment. For the bacteriaactive leaching experiments, 25 g of fresh plant (approximately half stems and half leaves, whole plant without cutting) or whole seagrass were added to each of a series of 2.5 l glass bottles containing 2.0 l of filtered seawater. Filtration of the seawater may have removed that portion of the bacterial community[0.7 lm, including those attached to particles (Bar-Zeev et al. 2012). This, however, was done because we were evaluating bacterial utilization of the dissolved phases of the ambient and leached organic matter only. Inclusion of the particulate phases would have complicated the interpretation of the results. For bacteriainhibited leaching experiments, 2.0 ml saturated HgCl2 solution was added to 1 l bottles, and the amount of plant material and water volume was reduced by a factor of two (12.5 g plant material in 1.0 l seawater) of that used in bacteria-active leaching experiments to generate less hazardous waste. The chemical composition of plant materials and seawater used for the incubation experiments are summarized in Table 1. All bottles were left open to the atmosphere (covered loosely with clean and baked aluminum foil) and incubated at room temperature (*25 °C) in the dark for 25 days. Water level was monitored during the experimental period, and analyzed concentrations were adjusted for water evaporation losses. At selected times (0, 1, 2, 3, 5, 8, 12, 17, 20 and 25 days), water samples were collected from each bottle and filtered for DOC, TDN, and CDOM fluorescence analysis. All glassware used in the sample collection and experimental process were acidcleaned, Milli-Q water rinsed and pre-combusted at 500 °C for 5 h. Chemical and fluorescence measurements Water samples collected from each bottle were filtered through pre-combusted 0.7 lm GF/F filters. Concentrations of DOC and TDN were measured using a Shimadzu TOC-VCPN analyzer to determine the leaching production of DOM from plants and seagrasses. The instrument was calibrated using 5-point carbon and nitrogen calibration curves derived from carbon standards using potassium hydrogen phthalate (KHP) and nitrogen standards using potassium nitrate (KNO3). All standards and samples were run in triplicate. Instrument blank and DOC values were checked against reference low carbon water and deep seawater (CRM, University of Miami, Rosenstiel School of Marine and Atmospheric Sciences). Blank subtraction was carried out using Milli-Q water, which was analyzed at regular intervals during sample analysis. Total blanks

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Table 1 Chemical composition of plant materials and seawater used for the incubation experiments Sample name

TOC (%) (dry wt.) TN (%) (dry wt.) C/N (g) Fresh wt (g) Dry wt (g) C added (mg) N added (mg)

April Spartina alterniflora

41.6

1.56

26.7

25

8.1

3,370

126

November Spartina alterniflora 40.2

1.09

36.9

25

11.2

4,502

122

April Juncus roemerianus

40.9

0.79

51.8

25

8.6

3,517

68

November Juncus roemerianus

43.2

1.01

42.8

25

14.2

6,134

143

April Syringodium filiforme

35.6

1.56

22.8

25

3.5

1,246

55

November Halodule wrightii

23.1

0.85

27.5

25

5.4

1,247

46

Seawater Salinity

25

DOC (lM)

480 ± 11

TDN (lM)

24.0 ± 2.4

CDOM (QSU)

38 ± 3

associated with DOC and TDN analyses were about 10 lM and 5 lM, and the analytical precision on triplicate injections was usually \3 %. CDOM fluorescence was determined as a measure of CDOM production during the plant leaching process. This measurement was conducted using a Photon Technologies International QM-1 spectrofluorometer. Single fluorescence emission scans from 350 to 650 nm were collected for an excitation wavelength of 337 nm. The fluorescence of Milli-Q water served as a blank, was determined on each day of analysis, and was subtracted from sample spectra prior to integration. Peak areas were integrated and converted to quinine sulfate units (QSU) where 1 QSU is equivalent to the fluorescence emission of 1 lg/l quinine sulfate solution (pH 2) integrated from 350 to 650 nm at an excitation wavelength of 337 nm (Chen and Gardner 2004). Reproducibility of these measurements was well under 1 % for seawater and incubation samples. CDOM absorption, another optically measurable characteristic of CDOM, was measured with a Cary 50 spectrophotometer after the samples were re-filtered through acid-cleaned 0.2 lm Poretics polycarbonate filters to remove any glass fibers that may have resulted from GF/ F filtration. Milli-Q water was used as a baseline reference, and CDOM absorption spectra (200–800 nm) were baseline-corrected by subtracting the 700–800 nm absorption assumed to be 0 (Chen and Gardner 2004). Absorption coefficients (a337) at 337 nm were calculated based on Stedmon et al. (2000) using the equation: a337 ¼ 2:303A=L

ð1Þ

where A is the measured optical density at 337 nm, and L is the cuvette pathlength in m. In a recent study, Helms et al. (2008) suggested that the CDOM absorbance spectral slope ratio (SR) calculated from two narrow wavelength ranges (275–295 and 350–400 nm) can be used as a good indicator of source and molecular weight of

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photo-bleached CDOM in coastal waters. We applied this approach to calculate S275–295 and S350–400 using linear regression of the log-transformed absorbance coefficients between 275–295 and 350–400 nm. SR is then obtained as SR ¼ S275295 =S350400 (Helms et al. 2008). In addition to single scan fluorescence data, we measured excitation–emission matrix spectroscopy (EEMs) for selected samples using a Hitachi F4500 fluorescence spectrophotometer. The purpose of EEMs measurement is to characterize, in general, the chemical composition of CDOM leached from different plants. Excitation wavelengths were varied from 250 to 500 nm in 5 nm increments. Emission wavelength data were collected from 260 to 600 nm in 5 nm increments. A normalized Milli-Q water EEM was collected and subtracted from sample data in order to remove the water Raman peak from the resulting EEM. All fluorescence data was instrument-corrected based on factory-supplied correction factors (emission correction at the factory, excitation correction during laboratory installation). All sample data were collected using a 1-cm quartz cuvette and are expressed in quinine sulfate units (QSU). An inner filter effect has been observed in samples above *100 QSU (Gardner et al. 2005) and may affect interpretation of both single scan and EEMs results. Therefore, samples above 100 QSU were diluted with Milli-Q water to eliminate this effect. Total organic carbon (TOC) and total nitrogen (TN) contents of the solid phases of the marsh plants and seagrasses were measured using a Perkin-Elmer 2400 CHN elemental analyzer. The plant and grass samples were dried at 50 °C and ground using a mortar and pestle and then analyzed for TOC and TN content. The analytical precision on duplicated analyses was ±4 % for TOC and ±5 % for TN. The dry weight of plants and grasses used for the experiment was determined after drying a known amount of fresh materials at 50 °C.


Results and discussion Leaching of DOC and TDN Leaching of DOC and TDN from salt marsh plants and seagrasses was a rapid process, and distinct differences of DOC and TDN leaching rates were found in the two incubation conditions (bacteria-active and bacteria-inhibited) as shown in Fig. 1. In the bacteria-inhibited incubations, concentrations of DOC leached from the plants and seagrasses increased rapidly, especially in the first 3 days (Fig. 1a). At the end of the experiments (Day 25), a wide concentration range of DOC, 1,600–7,200 lM were leached per gram of dry weight. April seagrass S. filiforme released the highest DOC concentrations and November seagrass H. wrightii had the lowest DOC release (Fig. 1a). The corresponding leaching rates were 65–288 lMC/g dry wt/day. In comparison to the bacteriainhibited incubations, the leached DOC concentrations in the bacteria-active incubations were much lower and relatively constant (Fig. 1b), in the range of 800–1,200 lM/ g dry wt (except a single point for April Syringodium on Day 7). The bacteria-inhibited leaching rates of DOC found here (19.2–86.4 g C kg-1 dry wt.) are comparable with the values (13.0–55.2 g C kg-1 dry wt.) reported by Maie et al. (2006) for bacteria-inhibited DOC leached from various wetland plants and seagrasses in NaN3-treated incubation experiments. The concentration of TDN in the bacteria-inhibited incubation also increased rapidly in the first 3 days and then slowly to the end of the experiment (Fig. 1c). April and November Spartina released much higher TDN concentrations (401 and 375 lM/g dry wt.; 16–15 lM/g dry wt./ day) than Juncus (96–177 lM/g dry wt.; 3.8–7.1 lM/ g dry wt./day) and the two seagrasses (111–156 lM/ g dry wt.; 4.4–6.2 lM/g dry wt./day). In contrast to the bacteria-inhibited case, concentrations of TDN in the bacteria-active incubations were 2–3 times lower (Fig. 1d). Again, Spartina had higher TDN release (160 lM/ g dry wt.) than other plants (50–68 lM/g dry wt.). The high leaching rates of DOC and TDN measured in our experiments provide clear evidence suggesting that salt marsh plants and seagrasses are important sources of DOC and TDN to marsh and coastal waters. When submerged in seawater, significant leaching of both DOC and TDN take place in 2–3 days, suggesting the rapid release of some biomolecules during initial hydrolysis. Some early studies of Spartina decomposition using litterbags in both field and laboratory experiments have demonstrated that the leaching and decomposition of S. alterniflora occurred in three phases (Lee et al. 1980; Valiela et al. 1985; Hicks et al. 1991; White and Howes 1994). An initial fast phase (days) of leaching soluble materials was followed by a second

599

phase (months) in which microorganisms gradually degraded the biopolymers and released soluble organic substances. The third phase took much longer (years), during which only refractory compounds such as cellulose and lignin remained. In their study of the decomposition of senescent seagrass H. wrightii in a subtropical lagoon in the US, Opsahl and Benner (1993) also reported a rapid loss of biomass carbon (36 %) during the initial leaching stage. Neutral sugars were the most abundant compounds produced during the hydrolysis of polymeric carbohydrate. The production patterns of DOC and TDN measured in our leaching experiment were likely controlled by the phase one and phase two leaching and decomposition processes. To further evaluate the leaching dynamics of DOC and TDN, DOC vs. TDN property–property plots show the leaching production from each plant in both bacteriainhibited and bacteria-active incubations (Fig. 2). Strong positive correlations (R2 = 0.90–0.99) between DOC and TDN were found for all samples in the bacteria-inhibited incubations, which suggests that leached plant carbon was generally proportional to leached nitrogen since all nitrogen released from the plant biomass should be mainly in organic form. However, variable C/N ratios were observed for different plants suggesting differing chemical composition of DOM released from each plant. Linear curve-fitting generated different C/N ratios (11.5–44.4) for the leachate produced from each plant. The chemical composition of DOM released from the plants appears not to be affected by seasonal life stages of the plants since DOM released from the April and November Spartina and Juncus grasses had similar C/N ratios (12.6 and 11.5; 27.7 and 26.2, respectively). These C/N ratios are much lower than their plant solid phase C/N ratios (26.7–36.9; 42.8–51.8), suggesting that more nitrogen than carbon in the plant tissues was released during the leaching process, or high N-containing organic compounds such as protein were released during the initial hydrolysis stage. For seagrasses, Halodule showed a lower C/N ratio for leachate (13.0) than solid phase (27.2), while DOM leached from Syringodium had a higher C/N ratio (44.4) than its solid phase value (22.8), indicating that carbon was released more rapidly than nitrogen for this seagrass. When bacteria were involved during the leaching process of each plant and seagrass, however, the C/N ratios of DOM varied dramatically and no clear correlations between leached DOC and TDN were found (Fig. 2). This indicates that bacteria play important roles in the preferential utilization of plant leached DOC and TDN and the bacterial production of DOC and TDN. The results of the bacteria-inhibited and bacteria-active incubations provide a direct comparison of leaching dynamics and the processes controlling DOC and TDN concentrations. In the bacteria-inhibited incubation, it is reasonable to assume that DOC and TDN concentrations

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Fig. 1 Leaching production of DOC and TDN from salt marsh plants and seagrasses is shown with incubation time. DOC leaching in a bacteria-inhibited and b bacteria-active incubations; TDN leaching

in c bacteria-inhibited and d bacteria-active incubations. The symbols are the same as shown in (b)

measured at the end of the experiment represent the total carbon and nitrogen chemically released from each plant. We calculated that DOC leached in seawater accounted for 5–14 % of the solid phase organic carbon for salt marsh plants Spartina and Juncus, 6 % for seagrass Halodule and 23 % for seagrass Syringodium (Fig. 3a). Concentrations of TDN accounted for 10–45 % of the plant solid phase organic nitrogen (Fig. 3a). Considering that the bacteriainhibited incubations were conducted in one liter of undisturbed seawater, the amounts of C and N chemically leached from each plant were quite significant. In natural salt marshes and coastal seagrass ecosystems with frequent water exchange and turbulence, the leaching dynamics and production rates could be even higher than under incubation conditions. In an early experiment, Turner (1993) performed leaching experiments on Spartina plants in a field setting in Louisiana coastal marshes and found that when S. alterniflora was submerged in seawater, the release rate of DOC was 15 times higher than in non-submerged plants. For the plant materials tested during the bacteriainhibited incubations, the % C released from the April and November Spartina were about the same, but April Juncus had much higher % C release than November Juncus. April

seagrass Syringodium had the highest C leached (23 %) out of all plants tested. Additionally, Spartina, Juncus, and Halodule leached more N than C. These leaching differences are likely related to the chemical composition and structure, and growth stage of the plants. As terrestrial vascular plants, Spartina and Juncus likely contain a high fraction of lignin in their stems and these high molecular weight compounds might not be easily chemically leached (Tukey 1970; Moran and Hodson 1990). Most of the carbon leached out was likely from the plant carbohydrates and proteins. In contrast to marsh plants, seagrasses Syringodium and Halodule do not possess strong, supportive stems. The structural component content should be lower in seagrasses, and their soft tissue celluloses contain high polysaccharide and low lignin compositions (Larkum et al. 1989). Polysaccharides should be more hydrophilic to dissolve in water than the hydrophobic lignin, supporting the high C/N ratio of DOM released from fresh seagrass Syringodium (Fig. 2). By measuring sugars and phenols concentrations, Maie et al. (2006) found that the quantity and quality of DOC leached from different wetland senescent plants varied significantly. Leaching yield of sugars from seagrass Cladium jamaicense was [2 times higher than that leached from marsh plants Eleocharis

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601

Fig. 2 Plot of DOC vs. TDN leached from the salt marsh plant and seagrass in bacteriainhibited and bacteria-active incubations. The line is a linear fit to the bacteria-inhibited incubation data and slope of the line represents C/N ratio of DOM leached from each plant

cellulose and Thpha domingenesis. For November seagrass Halodule, since we collected the brownish grass which was almost dead and floating on the sea surface, the grass could be significantly colonized by fungi and a large fraction of leachable carbon and nitrogen was probably lost already in the field. Rapid colonization during seagrass decomposition has been reported (Harrison 1989; Peduzzi and Herndl 1991). Microbial degradation of DOC and TDN Studies conducted in the field have demonstrated that bacteria play an important role in regulating the production, degradation, and distribution of DOC in salt marsh

systems (Valiela et al. 1985; Filip and Alberts 1988; Hopkinson et al. 1998; Moran et al. 1999). In our study, the concentration differences measured between the bacteriainhibited and bacteria-active incubations represent the amount of DOC and TDN being consumed by bacteria. We calculated that 56–90 % of the DOC and 37–72 % of the TDN were utilized by bacteria by the end of the incubation (Fig. 3b). Bacteria consumed more DOC than TDN during the respiration processes. However, during bacterial degradation of leached DOM, some DON were converted to DIN so it could result in under calculated TDN consumption. It appears that the removal of both DOC and TDN was a rapid process which occurred over the same time scales (1–3 days) as the leaching process. It should be pointed out

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a

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100

C

% Release

80

N

60 40 20 0 April Spartina Nov. Spartina

b

April Juncus

Nov. Juncus

Seagrass Syringodium

Seagrass Halodule

100

DOC

% Degradation

80

TDN

60 40 20 0 April Spartina Nov. Spartina

April Juncus

Nov. Juncus

Seagrass Syringodium

Seagrass Halodule

Fig. 3 Plot of a % of C and N leached from the solid phase salt marsh plant and seagrass; and b % of leached DOC and TDN being biodegraded at the end of the experiment

incubation (Fig. 2). Studies have shown that the tissue lignocelluloses of senescent and standing-dead marsh plants contain higher lignin content than that of fresh living plants (Hodson et al. 1984; Wilson et al. 1986). Labile compounds such as polysaccharides leached from marsh plants were degraded much faster than tissue lignin (Benner et al. 1984; Hodson et al. 1984). In their study, Scully et al. (2004) found that under oxic conditions, high concentrations of DOM, mainly high molecular weight (HMW) proteinaceous components derived from seagrass, were easily degraded by microbes, with polyphenol structures of plant-derived DOM being particularly sensitive to photo-oxidation. Benner and Hodson (1985) earlier reported that lignocelluloses derived from mangrove leaves and woody plants were more resistant to microbial degradation than lignocelluloses from marine macrophytes. The high degradation rates of DOC and TDN found in our experiments suggest that the freshly leached DOC and TDN from marsh plants and seagrasses were labile and important food sources to the microbial communities in salt marsh and coastal waters. This supports our field observations (unpublished data) that the majority of DOM produced in the salt marshes was recycled inside the marsh systems rather than being transported far offshore. Only a small fraction of outwelled CDOM and DOC were observed in offshore waters (Chen et al. 2013). Leaching and characterization of CDOM

that since GF/F filtered seawater was used for the incubations, bacterial abundance could be lower than that in natural seawater so the % of DOC and TDN degraded would be an underestimate. The quick removal of DOC and TDN leached from plants and seagrasses could have significant influence to carbon and nutrients cycles and other geochemical processes in natural salt marsh ecosystems. Studies have shown that the quality (i.e. bioavailability) of the carbon supply is a critical factor that must be considered when evaluating both the response of microheterotrophic communities and the ultimate fate of carbon within a system (Carlson and Ducklow 1996; Cherrier et al. 1996). Labile organic substrates and useable forms of inorganic and organic nitrogen promote bacterial production. In our experiments, bacteria consumed more DOC and TDN leached from April marsh plants and seagrasses than that leached from November samples, suggesting that DOM leached from the April fresh plants could contain a higher percentage of DON and/or low molecular weight (LMW) labile compounds than DOM leached from senescent plants collected in November. Also, the lower DOC/TDN ratios in the bacteria-active incubations than in the bacteria-inhibited incubations indicate that either DOC was consumed more rapidly than DON in most cases or that DON was converted significantly to DIN during the

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Outwelling of CDOM from salt marshes and seagrass beds into coastal waters can affect the quantity and quality of light available for photosynthesis by phytoplankton or benthic micro or macroalgae (Kelble et al. 2005). CDOM can also absorb UV light and produce reactive oxygen species that initiate photochemical reactions and affect biogeochemical cycles (Zepp 2002). Several studies conducted in the field found a positive relationship between CDOM fluorescence and DOC concentrations in estuarine and coastal waters (Vodacek et al. 1997; Ferrari 2000; Rochelle-Newall and Fisher 2002; Chen et al. 2004; Osburn and Stedmon 2011). The significance of increased CDOM as a result of a pulse of outwelled DOM from salt marshes during the fall is not currently known. During the leaching process in our experiments, it is clear that CDOM, measured as fluorescence intensity (QSU), was released significantly over time (Fig. 4a, b), and was proportional to the amount of leached DOC in the bacteria-inhibited cases (Fig. 4c) from both marsh plants and seagrasses. In the bacteria-inhibited incubations, fluorescence of CDOM increased with incubation time (Fig. 4a) and increased almost linearly with DOC leached from marsh plants and seagrasses. In comparison, fluorescence of CDOM in the bacteria-active incubations showed only a slight increase in


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Fig. 4 Measurement of CDOM production (as fluorescence) leached from salt marsh plants and seagrasses with incubation time in a bacteriainhibited and b bacteria-active incubations. And correlations of CDOM with DOC in c bacteria-inhibited and d bacteria-active incubations

the first 3 days and then remained relatively constant (45–75 QSU) during the rest of the incubation period. Correlations of CDOM fluorescence with DOC in the bacteria-active incubations were also limited and variable (Fig. 4d). Comparison of the optical properties of CDOM measured during the two sets of incubations provides an exclusive look at chemical leaching and the role of bacteria in regulating the CDOM production and removal processes. In the bacteria-inhibited incubations, since no bacterial activity is involved, CDOM fluorescence increases almost linearly with increasing DOC concentrations for each plant, indicating that CDOM is a major fraction of the DOM leached from the marsh plants and seagrasses. Note that this fraction could vary depending on the chemical composition of the DOM leached from each plant. In their study of DOM leaching from various plants and seagrasses collected from a Florida wetland, Maie et al. (2006) found that polyphenols leached from the plants could be an important source of CDOM and o-alkyl C was the major C form accounted for 55 ± 9 % of HMW fraction of CDOM leached from the plants. In our study, it appears that a significant fraction of CDOM was consumed by bacteria,

suggesting that much of the freshly leached CDOM is quite labile and bacteria could degrade freshly leached CDOM more rapidly than DOC in some cases. A pulsed plant source with a regulating function by bacteria clearly controls the quality and quantity of CDOM released from salt marshes and seagrass beds (Maie et al. 2006). Helms et al. (2008) used the slope ratio SR as an indicator of source and molecular weight of CDOM. They found that SR varied significantly for CDOM from different waters. CDOM produced in swamp, river, and estuarine waters had low SR values (0.88–1.50) compared to CDOM in the offshore (shelf break, 4.6) and open ocean (Sargasso Sea, 9.4) waters. A negative correlation between SR and CDOM molecular weight was also found with low SR generally related to the HMW CDOM. Our results showed that CDOM released from the April seagrass Syringodium and marsh plant Juncus had relatively higher SR values than CDOM leached from the other plants in both bacteriainhibited (Fig. 5a) and bacteria-active (Fig. 5b) incubations, suggesting that these fresh plants leached more low molecular weight (LMW) organic compounds to the DOM pool. These more degradable and lower C/N compounds appeared to have relatively low fluorescence intensity and

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Fig. 5 Plot of absorbance slop ratio SR vs. incubation time for CDOM leached from salt marsh plants and seagrasses in a bacteriainhibited and b bacteria-active incubations

degraded more rapidly than HMW substances. As additional HMW CDOM leached out or with more and more LMW organic compounds being utilized by bacteria with increasing incubation time, SR values gradually decrease toward the values of DOM measured in the Florida salt marsh waters (SR = 0.9–1.2). The patterns of SR support our DOC leaching patterns in the bacteria-inhibited and bacteria-active incubations as described above. EEM spectra of CDOM leached in the bacteria-inhibited incubations compared with bacteria-active incubations can provide further information on the chemical composition of DOM leached out from each plant and the chemical and structural changes under bacterial regulation. In an earlier study, Coble (1996) identified four significant peaks for EEM spectra of CDOM in coastal waters, corresponding to the excitation/emission wavelengths (nm) as follows: the H peak (260/380-460 nm) represents humic-like substances; the P peak (275/310 nm) is protein-associated DOM; the M peak (310/380-420 nm) is marine-derived DOM, and the T peak (350/420-480 nm) is terrestrially-derived DOM.

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As plotted for the April fresh plants in Fig. 6 and November senescent plants in Fig. 7 (all EEM samples were collected at the end of the incubations), it is clear that the protein-associated DOM (P peak) was a major fraction of CDOM released from Spartina and Juncus and especially for seagrass Syringodium in the bacteria-inhibited incubations. After bacterial degradation, the protein-associated CDOM was preferentially consumed in all cases, November Spartina showed a very strong peak in the Ex260–320/Em350–450 region covering both H and M peaks. April and November Juncus exhibited relatively high fluorescence intensities in the Ex265/Em350–450 region, mainly humic-like H peaks. The EEM spectral changes indicate that the bacterial reworking of DOM shifted the remaining CDOM to a longer wavelength associated with the humic-like H peak and marine-derived CDOM M peak. These changes again suggest the important bacterial control on the production, degradation, and distribution of DOM in the marsh and coastal waters. Several studies found that a similar red-shift occurs during the microbial degradation of DOM (Moran et al. 2000; Boyd and Osburn 2004). These EEM data are consistent with the results reported in our previous salt marsh plant decomposition study (Wang et al. 2007), indicating that substantial DOM leached from marsh plants and seagrasses are labile and highly biodegradable. These EEM data also demonstrate that bacteria play important roles not only in degradation of DOM but also in regulating the chemical and optical properties of DOM in the marsh and coastal waters. There also appears to be an increased production of humic substance CDOM (somewhere between M, H and T) for November grasses as they prepare for senescence relative to the April samples that are in full growth stages. Global implications of salt marsh and seagrass Salt marshes and seagrass meadows occupy a small fraction of the global landscape (*2 %), yet these combined wetlands represent one of the largest carbon reservoirs and one of the most active sites for carbon cycling (Adam 1990; Duarte et al. 2005). As summarized in Table 2, based on gross primary production (GPP) estimates, salt marshes are about twice as productive globally as seagrass meadows. However, when respiration (R) is accounted for in these ecosystems, the net ecosystem production (NEP) of both net autotrophic plant communities are about the same, 1 211–1,585 gC m-2 year-1, respectively, and therefore seagrass meadows and salt marshes are about equally important for carbon burial and/or carbon outwelling to the ocean (Duarte et al. 2010; Kennedy et al. 2010; Hopkinson et al. 2012). DOC production rates for salt marsh plants and seagrasses for our study region can be calculated based on the incubation studies presented in this paper. Using 25-day


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Fig. 6 EEM Spectra of CDOM leached from the April salt marsh plants and seagrass in bacteria-inhibited (left) and bacteria-active (right) incubations at the end of the experiment

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Fig. 7 EEM Spectra of CDOM leached from the November salt marsh plants and seagrass in bacteria-inhibited (left) and bacteria-active (right) incubations at the end of the experiment

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Table 2 Calculated outwelling fluxes of DOC and TDN from salt marsh plants and seagrass beds in the study coastal region in Florida Salt marshes

Seagrass beds

Area coverage (m2)

0.4 9 1012

0.3 9 1012

Gross primary production (gC m-2 year-1)

3,595

1,903

Globala

Respiration (gC m-2 year-1)

2,010

692

Net Production (gC m-2 year-1)

1,585

1,211

Florida big bend regionb Area coverage (m2)

6.65 9 108 -1

7.32 9 108

2.39 9 10

12

1.39 9 1012

Gross nitrogen production (g N year ) 6.08 9 10

10

6.10 9 1010

Gross primary production (gC year ) -1

DOC outwelling rate (gC m

-2

-1

year )

467

DN outwelling rate (g N m-2 year-1)

27.4

-1

DOC outwelling (gC year ) -1

TDN outwelling (g N year )

437 10.0

3.11 9 10

11

3.20 9 1011

1.82 9 10

10

0.73 9 1010

a For global, all values are from Duarte et al. (2005) and references therein

(Bar-Zeev et al. 2012), the utilization rate of DOC and DON in the natural salt marshes could be even higher. Salt marshes and seagrass meadows are important ecosystems that are facing significant losses globally due to climate change and anthropogenic influences (Sargent et al. 1995; Simas et al. 2001). Current predictions of sea level rise indicate increases of 0.75–1.90 m by the end of this century (Vermeer and Rahmstorf 2009). This sea level rise will inundate salt marshes and deepen waters over presentday seagrass beds. Inundation of salt marshes, in particular, could release a significant fraction of this labile DOC pool from the decaying plants over a short time period. This DOC release under rising sea levels represents a potentially major labile carbon source to the coastal ocean and carbon dioxide source to the atmosphere upon respiration that has yet to be included in our estimates of carbon cycle response and marine ecosystem resilience. Our DOC production rates indicate this wetland inundation source should be accounted for in future estimates of coastal ocean carbon budgets.

b

For Florida Big Bend Region, salt marsh coverage is from Montague and Odum (1997); seagrass coverage is from Sargent et al. (1995); gross primary production is calculated based on global GPP in Duarte et al. (2005); gross nitrogen production is based on C/N ratios measured for April Spartina and Juncus; DOC and TDN outwelling rates were calculated based on the leaching % of C and N measured at the end of the bacteria-inhibited incubations

DOC leaching rates (bacteria-inhibited) from the April fresh plants and seagrass as an annual rate (the lowest estimate), the estimated global GPP rate of 3,595 gC m-2 year-1for salt marsh and 1,903 gC m-2 year-1 for seagrass (Duarte et al. 2005 and references therein), and the mean TOC contents for the marsh plants and seagrass (Table 1), we calculate the production rates of DOC to be 467 and 437 gC m-2 year-1 for the salt marsh and seagrass beds, which account for 13 and 23 % of the global GPP of salt marshes and seagrass meadows (Duarte et al. 2005). Multiplying these by the areas of salt marsh and seagrass meadow at the Big Bend coastal region of Florida, the outwelling of DOC is estimated to be at least 3.11 9 1011 and 3.20 9 1011 gC year-1 from the salt marshes and seagrass beds. Similarly, we obtained the outwelling of TDN to be 1.83 9 1011 and 0.73 9 1011 gN year-1 from the salt marshes and seagrass beds. Seagrass meadows are about equally important as salt marshes as sources of DOC and TDN outwelling into the coastal waters in the region. However, the results from our study (bacteria-inhibited vs. bacteria-active) also indicate that [50 and [37 % of this DOC and DN were utilized by bacteria and recycled in marsh and coastal waters. It should be pointed out that because GF/F filtered seawater was used and may have reduced the bacterial abundances

Summary This plant incubation study demonstrates that salt marsh plants S. alterniflora and Juncus roemerianus, and seagrasses, S. filiforme and H. wrightii, are important contributors of DOC, TDN, and CDOM to the Florida salt marsh system and to the adjacent coastal waters in the Gulf of Mexico. The leaching of DOC, TDN, and CDOM is a rapid process when plants are submerged in seawater. Organic C and N were proportionally leached from the plants, but the quantity and quality of DOC and TDN production was related to the chemical composition, growth stage and structure of the plants. We found that the majority of DOC and TDN leached from marsh plants and seagrasses was labile and highly biodegradable. Rapid degradation rates suggest that bacteria play important roles not only in regulating the production and distribution of DOM but also altering the chemical and optical properties of DOM in the field. For the Snipe Creek, Florida salt marsh system from which these plants originated, we expect that the major fraction of DOM produced in the marsh waters is recycled within the marsh, and only a small fraction (\20 %) of refractory DOM could be transported to offshore waters and recycled over longer timescales of months to years. CDOM was proportionally leached along with DOC, but its fluorescence intensity and chemical composition varied with different plants. The EEM spectra indicate that the CDOM released from the marsh plants and seagrasses contained a significant amount of the protein-associated DOM that was degraded rapidly by bacteria. Leaching of

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DOM from the salt marsh plants and seagrasses provide not only major sources of DOC and CDOM, but also important food sources to microbial communities, thus serving an important pathway transferring vascular plant production to the microbial food webs and higher trophic levels in marsh and adjacent coastal waters. Acknowledgments We would like to thank Captain Gary Mears, Christof Meile, Bernie Gardner, Jill Arriola, Bridget Benson, Emily Gray, and Tom Heath for their help during the field sampling. We thank the two anonymous reviewers for their critical reviews and comments which improved the manuscript. This work was supported by the National Science Foundation (grant OCE-0928292 to RFC).

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