Rapid sediment accumulation and microbial mineralization in forests of the mangrove Kandelia candel in the Jiulongjiang Estuary, China

Estuarine, Coastal and Shelf Science 63 (2005) 605e618 www.elsevier.com/locate/ECSS

Rapid sediment accumulation and microbial mineralization in forests of the mangrove Kandelia candel in the Jiulongjiang Estuary, China D.M. Alongi*, J. Pfitzner, L.A. Trott, F. Tirendi, P. Dixon, D.W. Klumpp Australian Institute of Marine Science, PMB 3, Townsville M.C., Qld 4810, Australia Received 11 November 2004; accepted 19 January 2005

Abstract Rates of sediment accumulation and microbial mineralization were examined at three Kandelia candel forests spanning the intertidal zone along the south coastline of the heavily urbanized Jiulongljiang Estuary, Fujian Province, China. Mass sediment accumulation rates were rapid (range: 10e62 kg mÿ2 yÿ1) but decreased from the low- to the high-intertidal zone. High levels of radionuclides suggest that these sediments originate from erosion of agricultural soils within the catchment. Mineralization of sediment carbon and nitrogen was correspondingly rapid, with total rate of mineralization ranging from 135 to 191 mol C mÿ2 yÿ1 and 9 to 11 mol N mÿ2 yÿ1; rates were faster in summer than in autumn/winter. Rates of mineralization efficiency (70e93% for C; 69e92% for N) increased, as burial efficiency (7e30% for C; 8e31% for N) decreased, from the low-to the high-intertidal mangroves. Sulphate reduction was the dominant metabolic pathway to a depth of 1 m, with rates (19e281 mmol S mÿ2 dÿ1) exceeding those measured in other intertidal deposits. There is some evidence that Fe and Mn reduction-oxidation cycles are coupled to the activities of live roots within the 0e40 cm depth horizon. Oxic respiration accounted for 5e12% of total carbon mineralization. Methane flux was slow and highly variable when detectable (range: 5e66 mmol CH4 mÿ2 dÿ1). Nitrous oxide flux was also highly variable, but within the range (1.6e106.5 mmol N2O mÿ2 dÿ1) measured in other intertidal sediments. Rates of denitrification were rapid, ranging from 1106 to 3780 mmol N2 mÿ2 dÿ1, and equating to 11e20% of total sediment nitrogen inputs. Denitrification was supported by rapid NH4 release within surface deposits (range: 3.6e6.1 mmol mÿ2 dÿ1). Our results support the notion that mangrove forests are net accumulation sites for sediment and associated elements within estuaries, especially Kandelia candel forests receiving significant inputs as a direct result of intense human activity along the south China coast. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: sedimentation rates; diagenesis; carbon cycle; nitrogen cycle; organic matter; mangrove; sediment; China

1. Introduction The development of mangrove forests is closely intertwined with the dynamics of sediment transport, erosion, and accumulation along tropical and subtropical coastlines. The areal extent and species distribution

* Corresponding author. E-mail address: [email protected] (D.M. Alongi). 0272-7714/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2005.01.004

of mangroves is influenced by a variety of environmental gradients which respond to physical changes in sedimentary settings (Woodruffe, 2002). As land forms erode or accrete over time, mangrove vegetation will invariably respond with spatial and temporal changes in community patterns. Mangroves are influenced by, and in turn, modify sediment particle dynamics and chemistry. Mangroves develop in sheltered areas where fine sediments accumulate; the trees develop extensive root systems that actively capture silt and clay particles, and

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modify interstitial sediments and sediment chemistry via uptake and release of gases and solutes. These processes lead to the development of complex bacterial communities that are intimately associated with the decomposition of organic matter deposited with inorganic particles and secondarily with organic matter deposited over time from roots, leaf litter, and other organisms. The linkage between sediments and mangroves is thus tied to the cycling of carbon and nutrients within the forest floor. A few studies have examined nutrient cycling in relation to sediment accumulation in mangroves (Alongi et al., 2001, 2002, 2004; Holmer, 2003), especially in southeast Asia where 35% of the world’s mangroves are located. These studies revealed sediment accumulation rates more rapid than previous measurements from other locations (Twilley et al., 1992), and that efficiency of carbon and nitrogen burial was influenced by forest age and net forest primary production. These studies were located in areas receiving little to moderate human impact. Along the southern coast of China, the severity of impact on coastal habitats has increased dramatically since industrialization (Chua and Gorre, 2000), although subtropical estuaries have been affected by a variety of human disturbances for centuries (Elvin, 2004). In the Jiulongjiang Estuary in close proximity to the city of Xiamen, a wide variety of human activities have affected the ecosystem, as reflected by faecal coliform counts, heavy metal and inorganic nitrogen concentrations exceeding national standards (Chua and Gorre, 2000). Port development, mariculture, and rapid economic development have all contributed to areas of rapid siltation and erosion as well as an overall decline in environmental conditions. Mangroves in the estuary consist mostly of Kandelia candel forests replanted approximately 20 years ago in an effort to stabilize the coastline and to foster regrowth of mangroves and associated organisms (Lin, 1999). Several studies have examined the biology and cycling of some elements in these restored mangrove systems (Lin, 1999; Lin and Fu, 2000) but there is no data on sediment accumulation and the interplay between sediments and mangrove biogeochemistry for this region. This is unfortunate as China’s coastline resources are heavily used, and many provincial governments are now in the process of developing an integrated approach to coastal management. This study afforded us an opportunity to examine sediment-mangrove relations in an impacted subtropical estuary, especially in relation to differences in tidal elevation. Further, Kandelia candel is a mangrove tolerant of impacted environmental conditions, well suited for use in restoration of areas of north Asia’s coastline (Field, 1996), but little is known of its influence on sediment accumulation and biogeochemical cycles.

2. Material and methods 2.1. Study area The Jiulongjiang Estuary is located in Fujian Province (Fig. 1), which is the northern boundary of mangrove forests in China. The region is subtropical (mean annual temperature: 20.9  C), with most of the annual rainfall (1284 mm) derived from summer typhoons. The average annual temperature range of estuarine waters is from 14.8 to 27.8  C, with salinities adjacent to the mangroves ranging from 12 to 26. Tides are semi-diurnal with an average range of 4 m. Six species of mangroves occur in the estuary, but Kandelia candel is the canopy dominant. Most forests (z32 ha) are located on the southwestern shore where tidal flats are extensive. These forests were planted as part of several coastal restoration projects in the 1960s and 1970s. Station JJ1 (24  23.5# N, 117  54.3# E) was a mature Kandelia candel forest located in the high intertidal zone on the south bank of the estuary (Fig. 1), separated from large aquaculture ponds by a rock wall; pond effluents are intermittently discharged into the mangroves. Stations JJ2 (24  23.8# N, 117  54.3# E) and JJ3 (24  24.0# N, 117  54.1# E) were situated on the south bank of Da Tu Island (Fig. 1). Stn JJ2 was located in the mid intertidal zone seaward of aquaculture ponds on the island and composed mainly of densely planted Kandelia candel, with Aegiceras corniculatum as a minor species. Stn JJ3 was located in the low intertidal zone at the western end of the island, also seaward of aquaculture ponds. The stand was dominated by small Kandelia candel trees. The sites were chosen based on the intertidal zonation scheme of Alongi (1989). Sediment samples were taken in summer (July 2002) and autumn (September 2003). Only sulphate reduction was measured in winter (December 2003).

2.2. Forest and bulk sediment characteristics Within each forest, measurements for species identification, basal area and diameter-at-breast-height (DBH) using the angle count cruising method (Clough, 1997) were taken over a 100e200m2 area. All sediment samples were taken within these same plots. Biomass of fine roots was estimated from triplicate 1m-length cores taken at each site. Roots were washed of sediment and debris, and frozen until analysis. In the laboratory, roots were thawed and live and dead fine roots separated using the colloidal silica method of Robertson and Dixon (1993). For most microbial measurements, cores were taken to a sediment depth of 40 cm in July 2002 and to 100 cm in September 2003, except where noted below. Triplicate

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607

Fig. 1. Chart of the position of the three mangrove forests in relation to the entire Jiulongjiang Estuary, Fujian Province, China.

surface samples were taken by hand for percent sand, silt and clay, and water content (Folk, 1974). Solidphase concentrations of TOC, TN, TP, Fe, Mn and S were determined from 2e3 cores taken at each site to a depth of 1 m. Each core was cut at various intervals and processed as described in Alongi et al. (2001, 2002). The sediment slices were dried, ground and processed for total organic carbon and total nitrogen on a PerkinElmer 2400 CHNS/O Series II Analyser and a Shimadzu TOC Analyser with solid sampler. Other elements were determined after strong acid digestion on a Varian Liberty inductively-coupled atomic emission spectrometer following the procedure of Loring and Rantala (1992). Porewater was collected by siphoning water up from the holes left from sediment coring. The water was filtered (0.45 mm Minisart) using a sterile syringe and stored frozen until analysis. Sulphate in tidal water and porewater was determined gravimetrically by BaSO4 precipitation and filtration. Salinity was measured on filtered water by a hand-held refractometer. 2.3. Mass sediment accumulation Mass sediment accumulation rates were determined from gamma spectrometric measurements of 210Pb, 226 Ra and 137Cs made on sequentially sliced duplicate 95e100 cm-long cores taken at each site in July 2002 using a 1.5 m long (6 cm i.d.) stainless steel corer. Cores were taken equidistant from trees in order to minimize impacts from roots and crab burrows. Each core was cut

with a clean stainless steel cutting blade into 2 cm slices from the sediment surface to 20 cm depth, then into 4 cm slices to the bottom of the core. Gamma ray measurements were made on 50e150 g dried and ground sediment from each slice packed by a 10 metric ton hydraulic press into a custom designed gas-tight plastic container. Direct measurement of 210Pb was obtained from the 46.5 keV gamma emissions. After storage for 3e4 weeks, radon daughter in-growth allowed measurement of 226Ra from the gamma photopeaks of 214Pb at 295 and 351 keV, and 214Bi at 609 keV. Thermonuclear bomb fallout nuclide (137Cs) was measured from the 661.6 keV gamma emission of 137mBa. Four planar high-purity germanium detectors inside 10cm thick lead walled castles with steel liners were used for the gamma analysis. Energy spectra were calibrated with Amersham and CANMET standards of known low activity spikes of suitable nuclides in cleaned silica sand. IAEA marine reference material was used to check calibrations. Counting precision for 210Pb and 226Ra was %10%, but 137Cs precision approached 30% due to very low activities in these sediments. Interpretations of the radiochemical profiles were done with several sub-models incorporating weighted least-squares regression analysis (Robbins, 1978, 1979). These models utilize a sediment mixed layer thickness, a decadal-century scale average input of excess 210Pb (total 210Pb minus parent 226Ra), and diffusion coefficients for 210Pb and 137Cs in marine sediments (Li and Gregory, 1974). These MAR estimates were multiplied by average TOC and TN content in the same cores

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Table 1 Mean (G1 SE) forest and edaphic characteristics of the 3 Kandelia candel stands, Jiulongjiang Estuary, China

Tidal zone Basal area (m2 haÿ1) Tree density (stems haÿ1) Above-ground biomass (t haÿ1) DBH (cm) Salinity (psu) Percent sand Percent silt Percent clay Water content (%) TOC (% DW) TN (% DW) C:N (molar) TP (mg gÿ1) Fe (% DW) Mn (mg gÿ1) S (% DW)

JJ1

JJ2

JJ3

High 54

Mid 95

Low 41

48,256

143,644

79,903

133

93

16

5.6G0.2 17 2.2 56.6 41.2 31 1.77G0.14 0.12G0.008 17.7 509.8G25.0 4.45G0.17 592.2G9.5 0.61G0.07

4.4G0.1 14 1.7 56.3 42.0 33 1.02G0.08 0.077G0.006 15.4 573.9G13.3 5.09G0.13 1054.4G13.1 0.14G0.01

2.8G0.1 12 0.4 82.8 16.8 31 1.36G0.11 0.10G0.007 14.9 640.9G15.1 5.07G0.29 918.1G31.9 0.35G0.03

DBH, tree diameter-at-breast height; TOC, total organic carbon; TN, total nitrogen; TP, total phosphorus. Above-ground biomass was estimated using the allometric relationships in Tam et al. (1995).

(Table 1) to provide estimates of TOC and TN accumulation.

of 37% HCHO by injection with a fine needle to the bottom of each core, then flooded with ambient seawater after waiting for 30 min, closed and fitted to O2 probes to measure DO changes. Dissolved O2 flux in these poisoned chambers represents a rough estimate of chemical oxidation of reduced solutes diffusing from the sediment. Aerobic respiration (and possibly some chemolithotrophy) by organisms was estimated by the difference in DO flux rates between unamended and poisoned chambers. 2.5. Sulphate reduction To minimize compaction, intact cores for sulphate reduction were taken by inserting 120-cm long plastic tubes (2.7 cm diameter) into larger (6 cm i.d.) stainless steel cores as they were being inserted into the soil at low tide. The inner cores were extruded from the steel outer cores, capped with rubber stoppers, washed, and then injected with carrier-free 35S (Fossing and Jorgensen, 1989). Cores were injected at 2-cm intervals, incubated for 12e24 h, and then terminated by fixing sediments at 2-cm intervals in 20% zinc acetate. Samples were then frozen until a two-step distillation procedure was used to determine the fraction of reduced radiolabel shunted into the acid-volatile sulphide (AVS) and chromiumreducible sulphur (CRS) pools. 2.6. Fe, Mn and NHC 4 fluxes

2.4. CO2 and O2 fluxes Gas fluxes across the sediment-air interface were measured using one set of three semi-closed opaque chambers (volume: 1 L; area: 82 cm2) taken from each site at low tide in July 2002. Each chamber had a propellerelectric motor unit and two sampling ports on opposite sides of the chamber through which a stream of airflow was maintained by the propeller unit to minimize gas build-up. The chambers were incubated in a field laboratory in a shaded water bath maintained at ambient seawater temperature. Water was up to, but not over, the sediment surface in each chamber. Gas measurements were made via the airflow port connected to a MTI Analytical Instruments P200 gas chromatograph and checked using certified standards. All gas measurements were made every 30 min until a linear change was detected (usually 2e3 h). The detection limit was 0.045 mM. O2 flux was measured in September 2003 from identical opaque chambers submerged in a water bath with ambient seawater flowing over the entire unit. In one set of three chambers, dissolved oxygen was measured using O2 probes (TPSÔ Model WP-82 DO meters) placed into one sampling port. This flux represents total oxygen consumption (chemical oxidationCchemolithotrophyC aerobic respiration) from sediments. Another set of three opaque chambers were each poisoned with 100 ml

Rates of net dissolved Fe, Mn and NHC 4 release from sediments were measured in July 2002 (metals only) and September 2003. Briefly, triplicate sediment cores were taken at each site and cut into 15-cm portions. Each sediment cake was placed into glass jars and, in samples for metal release, mixed with 10 ml of Na2MoO4 (20 mM) solution. The jars were filled until no airspace was present. Sub-samples were taken before the jars were sealed, then squeezed for porewater (Alongi et al., 2001) and later analysed for total dissolved metals. The remaining sediment was incubated at in situ temperature for 3 days, then squeezed for porewater and processed on a Varian Liberty ICP-AES. Total NHC was 4 extracted from day 0 and day 3 samples by adding 10 KCl solution (1 N), incubated for 2e3 h, then squeezed to obtain total extractable NHC 4 . These nutrient samples were later analysed using automated techniques. 2.7. Denitrification, nitrogen fixation, methane and nitrous oxide fluxes Denitrification was measured from replicate sediment samples taken from each site using the N2 gas flux technique (Nowicki, 1994). Fluxes of methane and nitrous oxide were measured in the same chambers. Measurements were conducted in July 2002 and

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September 2003. Open-ended bottles were carefully pushed 6e10 cm into the sediment (volume: 230e385 cm3) so as to avoid large roots and other biogenic structures. Any obvious infauna was removed with tweezers before each sample was extruded into a gastight glass chamber (height 23.5 cm; i.d. 7.6 cm). Sediments in each chamber were covered with z 500e800 ml of creek water which was sparged with either 80%He/20%O2 mixture (4 experimental chambers per site) or 100% He (1e2 control chambers per site, see below) to remove N2 and, in the case of the experimental cores, to maintain dissolved O2 concentrations. The overlying water in each sealed chamber was stirred continuously. All chambers were incubated for 9 days in the dark at ambient temperatures to mimic field conditions as closely as possible. In the experimental chambers, the gas phase was flushed at 8-h intervals for the first two days with an 80%He/20% O2 mixture, and again, after the water overlying the sediment was periodically replaced with low-N2 seawater after day 3. The water exchange maintained O2 and an adequate NO3 supply in the experimental chambers for the duration of the experiment. The control chambers were incubated under anaerobic conditions (100% He gas flushes at 8-h intervals and deoxygenated water exchange) in order to block nitrification and denitrification (Nowicki, 1994). A 100% He- flushed, low N2 seawater exchange was carried out on day 3. After day 3, all control and experimental chambers were sealed and gas samples were withdrawn for measurement of O2,, CH4, N2O and N2 concentrations in the headspace. The accumulation of each gas in the headspace was measured each day for the next 5 days by withdrawing samples through the chamber ports with a He-flushed syringe. Samples were analysed using an MTI Analytical Instruments P200 gas chromatograph. Calibration standards were run with each set of samples using a certified gas mixture (1.99% N2, 20% O2, 0.021% N2O, 0.1% CH4, 77.889% He). Despite denitrification being blocked in the control cores, there can be significant de-gassing of N2 from the sediment porewater that diffuses into the overlying water and gas. This background flux of N2 (Fdg) measured in the control chambers was subtracted from the total N2 flux (Ft) measured in the experimental chambers to derive the rate of N2 flux due to denitrification (Fdn), where FdnZFtÿFdg (Nowicki, 1994). Denitrification rates were calculated as the average rate of triplicate cores from each site, from 3e4 individual incubation periods. CH4 and N2O accumulation rates in the gas headspaces were considered de novo synthesis and were calculated as the average rate of triplicate cores from each site using aerobic chambers only. Nitrogen fixation in sediments at each site was measured in three clear and two dark chambers using the acetylene reduction technique (Capone, 1993) in July

609

2002. Samples were taken by inserting open-ended chambers (surface area: 64 cm2) into the sediment to a depth of 5 cm. The chambers and soil plugs were then gently withdrawn with minimal disturbance. After return to the laboratory, the bases of the chambers were sealed with PVC end-caps containing an inert rubber plate. A 10% acetylene/air mixture was created (sediment volume: 320 cm3) and the headspaces were sampled immediately and at 3-h intervals, with a final sampling at z20 h. Acetylene and ethylene were analysed simultaneously by gas chromatography. The ethylene accumulation rates were converted to rates of N2 fixation using the theoretical factor of 4 C2H2 molecules equalling 1 N molecule (Capone, 1993).

3. Results 3.1. Forest and sediment characteristics All three forests were characterized by dense assemblages of K. candel, with trees most dense at Stn JJ2 (Table 1). Trees were largest at Stn JJ1 and of smallest diameter at Stn JJ3. Interstitial salinity ranged from 12 to 17 among sites with no clear differences between sampling intervals. Sediments at all three sites were composed mostly of silt and clay with little sand, with 31e33% water content (Table 1). Living tree roots were found mostly within the 10e40 cm sediment interval with most live roots at Stn JJ2 and the least at Stn JJ3 (Fig. 2); comparatively few live roots were found below 50 cm depth. Dead roots were more erratically distributed with sediment depth, but greater in concentration than live roots (Fig. 2). Total organic carbon and total nitrogen concentrations (Fig. 3) were greater at Stn JJ1 (Table 1), especially over the upper 40 cm horizon; concentrations were lowest at Stn JJ2. C:N ratios were highest at Stn JJ1 and lowest at Stn JJ3 (Table 1). Total P concentrations declined with increasing tidal elevation, but concentrations of Fe were equivalent at Stns JJ2 and JJ3, with the least Fe at Stn JJ1. Vertical profiles of Fe indicate increasing concentrations below the maximum live root zone at all three sites (Fig. 3). Sulphur concentrations similarly increased with sediment depth at Stns JJ1 and JJ3; concentrations of S were lowest at Stn JJ2 and highest at Stn JJ1 (Table 1). Mn concentrations peaked in surface sediments at all three sites (Fig. 3) and were highest at Stn JJ2 and lowest at Stn JJ1 (Table 1). 3.2. Sediment accumulation rate estimates The excess 210Pb profiles from both cores from Stn JJ1 allowed a reasonable estimate of mass accumulation rate (MAR) of 9.6 G 2.5 kg mÿ2 yÿ1 with a sediment mixed layer thickness (MLT) of 9e20 cm (Table 2). This

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inventory of these isotopes were greater than twice that expected from atmospheric supply, and the inventory was not complete for 210Pb due to lack of deeper slices. The bomb fallout 137Cs profile in core 3563 was incomplete, so this isotope was not used to support the interpretation of MAR for this core. The excess 210Pb profiles from the two cores from Stn JJ3 were problematic and difficult to interpret, as the inventories were incomplete (Fig. 4C), indicating that the cores were not long enough. Model estimates of the scatter of data points for excess 210Pb suggest a very high MAR for both cores of 62G25 kg mÿ2 yrÿ1 (Table 2). Modelling of the excess 210Pb profiles indicate a mixed layer thickness of 1e2 cm, but the bomb fallout 137 Cs profiles suggest that a large amount of labelled material deposited over a short time span (Fig. 4C), with half the bomb fallout history being absent due to lack of core length. Large variations in the 137Cs profiles do not support the idea of complete mixing down-core, as highly mixed sediments would have low layer-to-layer variation. There was very high excess 228Th activity in the top 14e15 slices (Fig. 4D) supporting the very high accumulation rate interpretation. 3.3. Flux estimates of CO2, O2, CH4 and N2O

Fig. 2. Vertical profiles of live and dead roots to a depth of 100 cm, July 2002. Values are meanG1 SE.

MLT must represent relatively slow or episodic mixing, as high activities of excess 228Th excess were found in the top 7e15 slices (data not shown). The very good core profiles (Fig. 4A) of bomb fallout 137Cs were in rough agreement with the excess 210Pb profiles, suggesting that sediment down to 85 cm depth is labelled with post-1950 bomb nuclides. At z85 cm depth there was a discontinuity in the profiles, as the sediment appears to be significantly older, as indicated by the lack of 137Cs and steep decline in 210Pb excess activity (Fig. 4A). Visual observations indicated a clear boundary between mangrove-associated silt-clays and compacted fine sand at this depth interval. The excess 210Pb profiles from the two cores from Stn JJ2 indicated a mean mass accumulation rate of 20.4G4.0 kg mÿ2 yÿ1, with a relatively thin sediment mixed layer of 3e7 cm (Table 2). The top 7e8 slices had excess 228Th (data not shown), which suggests little sediment mixing in the last decade. The bomb fallout 137 Cs profiles (Fig. 4B) show a good curve expected from atmospheric supply history, but the maximum 137 Cs activities have been spread upward in core time, perhaps due to sediments labelled with high 137Cs activity arriving from the catchments. The whole core

The rates of CO2 flux (Table 3) ranged from 17e40 mmol mÿ2 dÿ1 in summer to values of 103e121 mmol mÿ2 dÿ1 in autumn. These values are not directly comparable owing to the different methods used, but suggest roughly equivalent rates of CO2 release from surface sediments among sites. Rates of dissolved O2 flux were also equivalent among sites with estimated rates of chemical oxygen demand accounting for an average of 60% of total oxygen demand in autumn (Table 3). Rates of O2 gas flux in summer were more rapid than DO fluxes in autumn (Table 3). Rates of methane and nitrous oxide release were highly variable across sites and seasons (Table 3). 3.4. Denitrification and nitrogen fixation Rates of denitrification were rapid, ranging from 1106 to 3780 mmol N2 mÿ2 dÿ1 (Table 4). Denitrification was more rapid in summer at Stns JJ1 and JJ3. Nitrogen fixation was measured only in summer at Stn JJ3 (Table 4). 3.5. Net metal and NH4 release Maximum rates of net Fe and Mn release (Table 5) coincided with peak densities of live roots (productmoment rZC0:89; P!0:05, all sites), especially at Stn JJ2 where live root density was highest. Rates of Mn release were higher in autumn than in summer at equivalent depth of 40 cm. Fe release was detected only in autumn (Table 5). NHC 4 release was measured only in

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611

Fig. 3. Vertical profiles of total organic carbon, total nitrogen, total phosphorus, manganese, iron and sulphur to a depth of 100 cm, July 2002. Values are meanG1 SE.

autumn and was equivalent among sites (Table 5), ranging from 3.6 to 6.1 mmol N mÿ2 dÿ1. 3.6. Sulphate reduction Depth-integrated rates of sulphate reduction were highest in summer and lowest in winter (Table 6) at all

three sites. Most 35S was incorporated into the CRS fraction, with highest recovery in the AVS fraction at Stn JJ3. Sulphate reduction was measurable to a depth of 1 m at all three sites (Fig. 5). Site differences were inconsistent, with equivalent rates in summer but slowest rates in autumn at Stn JJ2 and in winter at Stn JJ1 (Table 6).

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Table 2 Bulk sediment mass accumulation (MAR, kg mÿ2 yÿ1), excess 210Pb atmospheric flux (Bq mÿ2 yÿ1) necessary to support the core profiles, core depth-integrated inventory of S137Cs (Bq mÿ2) and sediment mixed layer thickness (cm) in cores taken for the three mangrove sites, July 2002 210

Site

Core no.

MAR

Excess

JJ1 JJ1 JJ2 JJ2 JJ3 JJ3

3560 3561 3562 3563 3564 3565

8.4G2.0 10.7G3.0 19.5G4.0 21.2G5.0 75.0G30 49.0G20

1491G195 1238G204 1440G169 1572G188 2260G193 1841G147

Pb

S137Cs

Mixed layer

2937G506 2708G508 3280G523 4200G607 2565G612 1889G376

20 9 7 3 !2 !1

3.7. C and N sediment budgets The mean contribution of each of the various metabolic pathways to total microbial metabolism was estimated by averaging seasonal values for each process and converting to carbon equivalents assuming standard diagenetic equations (Table 7). The estimates indicate that sulphate reduction is the major decomposition pathway, with aerobic respiration being the second major process. Rates of total carbon metabolism range from 518 to 624 mmol C mÿ2 dÿ1 in summer and from 219 to 420 mmol C mÿ2 dÿ1 in autumn (Table 7). By using average rates of metabolism and sediment accumulation, budgets of sediment organic carbon and

Fig. 4. Vertical profiles of excess 210Pb and 137Cs activity in relation to sediment depth (g cmÿ2) in (A) core 3560 taken at Stn JJ1, (B) core 3562 taken at Stn JJ2, (C) core 3564 taken at Stn JJ3, and (D) excess 228Th activity in core 3564, July 2002. Activities are expressed in Bq kgÿ1 sediment DW. Diagonal line represents best-fit model for 210PB activity below the mixed depth.

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613

Fig. 4. (continued)

nitrogen were constructed (Table 8). The carbon budgets indicate that mineralization efficiency increases, and burial efficiency decreases, with increasing tidal elevation. There is proportionally greater carbon burial in the low intertidal zone where sediment accumulation was greatest. The pattern is similar for nitrogen, with greater mineralization efficiencies with increasing elevation, but greater N burial at Stn JJ3. The percentage of total nitrogen input denitrified ranged from 11% to 20% (Table 8).

4. Discussion 4.1. Rates of sediment accumulation Rates of mass sediment accumulation and carbon burial in mangrove forests vary widely, although Twilley et al. (1992) calculated a mean burial rate of carbon of 8.3 mol C mÿ2 yÿ1. More recently, Saenger (2002) estimated that vertical accretion in mangroves commonly approaches 0.5 cm yÿ1. In our study of the Chinese

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Table 3 Flux rates (meanG1SE) of (A) CO2 gas and SCO2, (B) O2 gas and dissolved O2 in unamended and poisoned chambers, (C) CH4, (D) N2O in July and September 2002 JJ1

JJ2

40G14 103G42

17G14 116G29

37G12 121G30

83G13

79G20

123G32

56G14 37G8

57G9 37G10

51G6 25G3

(C) CH4 Summer Autumn

66G98 0

11G18 0

0

(D) N2O Summer Autumn

1.9G1.0 0

1.6G0.3 0

106.5G158.2 5G4

(A) CO2 Summer (gas) Autumn (aq) (B) O2 Summer (gas) Autumn Unamended Poisoned

JJ3

5G4

Values in (A) and (B) are mmol mÿ2 dÿ1 and mmol mÿ2 dÿ1 for methane and nitrous oxide.

mangroves, sediment accumulation rates were rapid compared with the above-cited averages and with estimates from our earlier work in Thailand (Alongi et al., 2001) and Malaysia (Alongi et al., 2004). We calculated that mass accumulation rates decreased from the low-intertidal to the high-intertidal forests, with average rates from 49e75 kg mÿ2 yÿ1 in the lowintertidal stand (Sta. JJ3) to 8e11 kg mÿ2 yÿ1 at the high-intertidal forest. These equate to accretion rates of 6e10 cm yÿ1 at Stn JJ3 to rates of 1.3e1.4 cm yÿ1 at the high-intertidal stand (Sta. JJ1). Using decadal changes relative to mean tidal datum, Lu and Lin (1993) estimated a sedimentation rate of 3e4 cm yÿ1 in a location adjacent to Stn JJ1, confirming rapid sedimentation in the intertidal zone. All six cores taken for radiochemistry revealed exponential decay profiles of 210Pb in excess of 226Ra activity for estimated average annual 210Pb fluxes ranging from 1238 to 2260 Bq mÿ2 yÿ1, approximately 3e5 times the supply rate from the atmosphere (Turekian et al., 1977; Feichter et al., 1991). This can be interpreted as focusing of fine sediment from a larger Table 4 Rates of denitrification and nitrogen fixation (mmol N2 mÿ2 dÿ1) as measured in chambers using the direct gas technique at the three sites JJ1

JJ2

Denitrification Summer Autumn

3264G768 1106G639

2472G264 3780G2229

Nitrogen fixation Summer

0

0

N2 fixation was measured only in July 2002.

Table 5 Total mean (G1 SE) rates of net Mn, Fe and NHC 4 release in amended incubations at various sediment intervals in each mangrove forest JJ1

JJ2

JJ3

Mn Summer (0e40 cm) Autumn (0e100 cm)

2.2G0.5 16.8G14.1

2.7G0.7 38.6G8.9

3.8G1.6 29.1G17.6

Fe Autumn (0e100 cm)

37.2G9.2

45.3G14.3

2.6G0.4

NHC 4 Autumn (0e30 cm)

6.1G3.2

3.6G1.5

4.3G1.7

Values are expressed as mmol mÿ2 dÿ1. In July 2002, net Fe release was not detected at any of the sites, and NHC 4 release was not measured.

area of sediment transport to a small area of deposition. This idea is supported by observations of sediment movement in the estuary that imply high rates of terrestrial soil transport from the Jiulongjiang River as well as localized transport of coastal sediments from east to west (Chua and Gorre, 2000). It is important to note that our rates are coarse estimates, especially for Stn JJ3, where longer cores would be necessary to capture the entire inventory of radionuclides. For this reason, our values have comparatively large standard errors in the models, and so must be considered with caution. The inventories of bomb fallout 137Cs (Table 2) and of 228Th and parent 228Ra (data not shown) are several times greater than the expected fallout for this region (UNSCEAR, 1977), suggesting rapid deposition such that these sediments have not been exposed long enough for substantial mixing and desorption by seawater to occur. These inventories also suggest that these sediments are more likely to originate from surface soils within the catchment than from the sea. This is a reasonable idea given the intense agriculture and high rates of soil erosion within the province (ITTXDP, 1996). The high sedimentation rates may also be caused by the unknown amounts of waste dumped from the aquaculture ponds located behind the mangroves, as well as enhanced deposition from intense sand dredging in the adjacent waterways. Our estimates are not absolute, but do clearly show that there is a feedback process between sedimentation and mangrove Table 6 Depth-integrated rates of bacterial sulphate reduction (mmol S mÿ2 dÿ1) and proportion of radiolabel incorporated into the acidvolatile fraction (%AVS) at the three forests in July 2002, and September and December 2003 JJ1

JJ2

JJ3

Summer (40 cm)

281G49 (3%)

231G66 (4%)

224G64 (11%)

Autumn (40 cm) Autumn (100 cm)

115G48 191G57 (3%)

43G18 81G32 (4%)

73G17 161G36 (12%)

19G4 46G13 (2%)

31G10 59G20 (2%)

44G10 114G26 (8%)

JJ3 3120G624 1963G1019 42G45

Winter (40 cm) Winter (100 cm)

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Table 7 Mean contribution of the various carbon oxidation pathways (mmol C mÿ2 dÿ1) to total carbon metabolism at each of the three stands to a depth of 40 cm in summer and 100 cm in autumn JJ1

JJ2

JJ3

Summer (0e40 cm) O2 Denitrification Mn reduction Fe reduction SO4 reduction Methanogenesis SC oxidation

55 6 1 0 562 0.07 624

51 5 1 0 462 0.01 519

62 6 2 0 448 0 518

Autumn (0e100 cm) O2 Denitrification Mn reduction Fe reduction SO4 reduction Methanogenesis SC oxidation

19 2 8 9 382 0 420

20 8 18 11 162 0 219

26 4 13 1 322 0.005 366

All conversions to carbon were made using the diagenetic equations in Canfield (1993). Aerobic respiration estimated by subtracting chemical oxygen demand (poisoned chamber values) from rates of gross oxygen demand (unamended chambers). Values are means.

may be counterbalanced by erosion of some intertidal areas by heavy ship traffic. The mangrove forests in this estuary are unlikely to be growing in a steady-state environment given the variety of human disturbances (Lin and Fu, 2000). 4.2. Rates and pathways of microbial decomposition

Fig. 5. Vertical profiles of total rates of sulphate reduction, July 2002 (40 cm), September 2003 (100 cm) and December 2003 (100 cm). Values depict meanG1 SE.

formation; sedimentation rates decline as mangroves and soils horizons develop up to mean high tide (Woodruffe, 2002). Visual and satellite observations of both Hainan and Da Tu islands indicate that these two islands have now joined and are currently prograding at both ends, where Stn JJ3 was located. The rate of mangrove formation induced by the high accretion rates

The rates of microbial mineralization correspond to the rapid sedimentation rates, ranging from 135 to 191 mol C mÿ2 yÿ1 over a sediment depth interval of 1 m. This range of total C mineralization exceeds those measured in other mangrove deposits (Holmer, 2003) and in salt marshes where highest rates range from 108 to 185 mol C mÿ2 yÿ1 (Howarth, 1993). The bulk of the carbon oxidation was performed by sulphate reducers with comparatively modest oxidation by aerobic bacteria, denitrifiers, metal-reducing bacteria and methanogens. Compared with the well-known relationship between sediment deposition rate and mineralization in other marine sediments (Canfield, 1993; Henrichs, 1993), our values are well within the boundaries of the relationship. However, the contribution of sulphate reduction appears to greater than expected from the relationship as compiled in Fig. 6 of Canfield (1993). This reflects the fact that rates of sulphate reduction were consistently rapid to a depth of 1m. Our values are among the highest recorded for intertidal deposits, ranging from 60 to 200 mol C mÿ2 yÿ1 (Tables 6 and 7) as compared with salt marsh values ranging from 12 to 150 mol C mÿ2 yÿ1 (Giblin and Wieder, 1992).

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Table 8 Estimates of sediment organic carbon and total nitrogen input (mol mÿ2 yÿ1), and mineralization and burial efficiencies (%) at the three mangrove forests JJ1

JJ2

JJ3

Carbon POC buriala C mineralizationb Total C inputc Mineralization efficiencyd Burial efficiencye

14 191 205 93% 7%

17 135 152 89% 11%

70 161 231 70% 30%

Nitrogen TN buriala Total N mineralizationb Total N inputc Mineralization efficiencyd Burial efficiencye % T N input denitrifiedf

1 11 12 92% 8% 16%

1 9 10 90% 10% 20%

5 11 16 69% 31% 11%

See footnotes for equations and assumptions in calculating these values. Figures are derived averaging seasonal values where possible. a Rates of POC and TN accumulation derived by multiplying mean sediment accumulation rates (Table 2) by mean POC and TN concentrations in sediments (Table 1). b Mean of C data in Table 7 and N mineralization estimated by dividing C mineralization by mean molar sediment C:N ratio (Table 1). c Derived using the steady-state equation, EINZEOUTC EACCUMULATION (Berner, 1980). This equates to summing burial and mineralization rates. d Mineralization/Total Input!100. e Burial/Total Input!100. f Mean denitrification rates (Table 4)/Total N Input!100.

In most other sedimentary environments, sulphatereducing activity usually peaks a few cm below the sediment surface after oxygen, NO3, MnO2 and Fe2O3 are depleted via the well-known diagenetic sequence. In mangrove deposits, particularly those in meso- and macro-tidal environments, microbial activity can persist to sediment depths of at least 1 m (Alongi et al., 2001). This is thought to be a response to exudation of solutes and gases via roots that in some large trees can often exceed a depth of 2e3 m. Further, vertical expansion of the zones of diagenesis can be fostered by the movements of rain and tidal waters through the sedimentary facies via crab burrows, holes, cracks and fissures. These interstitial waters may then be gravitationally flushed laterally at low tide, or percolate up on the flood tide. Evidence for lateral movement of interstitial waters is provided by visual observations and random sampling of pore water draining laterally at the interface between forest floor and the low tide mark. This idea may help to explain why the gas and solute measurements taken from chambers containing surface sediments (Table 3) were significantly less than the total C mineralization rates estimated from the sum of the individual decomposition processes (Table 7). In July 2002, we analysed these waters for SCO2 and found concentrations equivalent with those of the pore water (meanZ28 mM of nZ3 at each site) and significantly

greater than in the estuary (meanZ0:9 mM, nZ10). It is therefore likely that CO2 and other gases and solutes are lost via lateral flow during ebb and flood tides. The lower rates of CO2 gas flux from surface sediments compared with the sum of the individual processes may also not only be from losses as a result of lateral transport, but also because of CO2 consumed during authigenic mineral formation and losses via chemotrophy by sulphide oxidizers. The latter is very probable given the very high rates of sulphate reduction leading to strong production of sulphide. The formation of minerals such as FeCO3 is possible given the high concentrations of solid-phase iron associated with dead roots. In any event, the measurement of gases across the sedimente airewater interface is likely to underestimate the true rates of microbial activity in deeper sediments, especially if early diagenesis is not in steady-state. Such may be the case in these sediments where large tides and disturbances, such as aquaculture wastes, may facilitate oxidation in surface sediments (e.g. Mn oxides) and trapping of elements into solid-phase (e.g. Fe, S), or both; interstitial water and gas movements were probably greater than rates of either molecular or ionic diffusion or biological advection, as oscillations in sediment conditions can disrupt steady-state diagenesis (Aller, 1994). Our estimates of aerobic respiration were crude owing to the lack of a direct method of measurement. We presume that the difference in oxygen demand between the unamended and poisoned chambers represents mostly oxic respiration. The chamber measurements account only for respiration in the surface sediments and do not account for possible oxic respiration associated with subsurface roots and the linings of other biogenic structures. Similarly, the rates of other gas fluxes were taken from the chambers for denitrification and only account for flow within the sediment depth of roughly 10 cm. In most marine sediments, methanogenesis occurs in deeper deposits below the zone of sulphate depletion, so it is likely that we underestimated the rate of methane efflux. Compared with the few studies that have measured CH4 flux in mangroves, our rates are low and highly variable. For instance, Sotomayer et al. (1994) measured methane fluxes in Puerto Rican mangroves within the range of 0.25e5.1 mmol C mÿ2 dÿ1. The low rates of methane efflux in these Chinese mangroves also probably reflect the dominance of sulphate reducers. The rates of Fe and Mn release were underestimates of rates of iron and manganese reduction, as there are no methods to measure these processes directly. Nevertheless, our data do show that release of dissolved metals coincides with the zones of maximum live root biomass. Several studies have indicated a close association between metal cycling and roots (Lacerda et al., 1993) to the extent that iron and manganese

D.M. Alongi et al. / Estuarine, Coastal and Shelf Science 63 (2005) 605e618

co-precipitate as plaques on root surfaces, as found on other aquatic plant roots (Sundby et al., 1998). As in an earlier study in Thailand (Alongi et al., 2004), concentrations of Fe and Mn in live and dead roots were high compared to other plants (Drechsel and Zech, 1993), with percent iron ranging from 1.7% to 3.7% in live roots and from 7.6% to 8.4% in dead roots; Mn concentrations were also higher in dead roots, ranging from 1070 to 3000 mg gÿ1 compared with 390e650 mg gÿ1 in live roots (three sub-samples taken from roots at all three sites). The higher concentration of metals in dead roots suggests that dead roots are loci for pyrite formation and trace metal precipitation. Vertical profiles of Fe and S (Fig. 3) show a build-up of both metals with increasing sediment depth at some sites, probably the result of both pyrite formation via sulphate reduction and the formation of metal concretions from precipitation of insoluble oxides in living rhizospheres and FeS2 on dead roots. Vertical profiles of Mn suggest oxidation and precipitation in surface sediments (Fig. 3) which may be the net result of diffusive transport of reduced Mn to the sediment surface. 4.3. Nitrogen transformations Nitrogen cycling appears to be equally rapid in these deposits, with mineralization efficiencies ranging from 69% to 92% (Table 8). As with carbon, burial efficiency of nitrogen declined with increasing tidal elevation. Fluxes of nitrous oxide (Table 3) were highly variable but within the range measured in other mangrove environments (Corredor et al., 1999) supporting the concept that mangrove forests constitute a significant global source of N2O. Rates of denitrification (Table 4) were very rapid compared with other mangrove estimates (Rivera-Monroy and Twilley, 1996) mirroring rates of net ammonification (Table 5), especially during summer when warmer temperatures stimulated microbial activity. Few measurements of ammonification are extant for mangroves, but the available data indicate that the source of NO3 for denitrification is via transformation by ammonification and nitrification, rather than via NO3 uptake from tidal water. The high rates of denitrification imply anthropogenic N inputs (Seitzinger, 1988), such as from the aquaculture ponds, but the percentage of total nitrogen input denitrified ranged from 11% to 20%, which is within the percentage range from unpolluted estuaries (Seitzinger, 1988). Our rapid rates of nitrogen mineralization agree with estimates of rapid cycling in other mangrove deposits (Holmer, 2003). 4.4. Nutrient budgets The sediment carbon and nitrogen budgets are subject to considerable uncertainty, but support the

617

notion that mangrove sediments are able to conserve and retain essential elements, as suggested for element retention in other mangrove ecosystems (RiveraMonroy and Twilley, 1996; Holmer, 2003). The results from these Chinese mangroves support the concept that mangrove sediments are accumulation sites for fine sediment, carbon and nutrient elements. Lin (1999) estimated net primary production for Kandelia candel of 57 mol C mÿ2 yÿ1 and net nitrogen retention of 0.5 mol N mÿ2 yÿ1 in stands very similar in size to those sampled at Stns JJ1 and JJ2. This production figure is remarkably close to the global mangrove NPP average of 58 mol C mÿ2 yÿ1 (Gattuso et al., 1998). Comparing the NPP to the net burial rates (Table 8), it is clear that C burial in sediments at Stns JJ1 and JJ2 equate to 26e30% of tree carbon production. Lin (1999) also estimated a net tree N production as 0.5 mol N mÿ2 yÿ1, which is roughly one-half of the estimated sediment N burial rates. Comparing tree C and N production with sediment mineralization, rates of carbon oxidation in sediments are 2e3 times greater, and rates of nitrogen mineralization are roughly 20 times greater, than element accumulation in the trees. This suggests that carbon and nitrogen cycling in these deposits are determined mainly by rates of mass sediment accumulation and other environmental factors (e.g., temperature), with the influence of tree growth and production restricted mostly to the maximum depth of penetration of live roots, which appear to play a key role of iron and manganese cycling. Nevertheless, our results of rapid carbon and nitrogen cycling support earlier notions that Kandelia candel is tolerant of dramatic chemical and physical changes to sedimentary facies along the south China coast. Acknowledgements This study was supported by a grant from the Department of Industry, Science and Technology, Canberra, Australia, the Australian Institute of Marine Science, and Greenfields Pty Ltd. We thank Ben Quinn for his help and assistance in providing resources in support of this research.

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