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The origin of the suspended particulate matter in the seagrass meadow of tropical waters, an evidence of the stable isotope signatures
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A’an Johan WAHYUDI1, *, AFDAL1
Acta Oceanologica Sinica | 2019, 38(1) : 136 - 143
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Acta Oceanologica Sinica | 2019, 38(1): 136-143
• Marine Biology •
The origin of the suspended particulate matter in the seagrass meadow of tropical waters, an evidence of the stable isotope signatures
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A’an Johan WAHYUDI1, *, AFDAL1
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  • 1 Research Center for Oceanography, Indonesian Institute of Sciences, Jakarta 14430, Indonesia
Published: 2019-01-25 doi: 10.1007/s13131-019-1380-z
Outline
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Suspended particulate matter (SPM) has been known as an important variable in the organic matter flow of coastal ecosystem. Half of burial carbon in seagrass meadows is contributed by allochthonous sources that compose the SPM such as phytoplankton, seagrass detritus, marine snow aggregates and terrestrially derived particles. Each composition of the SPM contributes different roles and is important to be identified, for instance, the exact contribution of seagrass detritus will be useful for determination of carbon export through the detritus form in seagrass meadows. Here, the SPM of seagrass meadows is studied in Bintan Island and the Selayar Archipelago. The aim of this research is to determine the source origin of the SPM using a stable isotope signature. In order to fulfill this aim, the objectives are defined as: (1) to specify the stable isotope signature (δ13C and δ15N) of the SPM, and (2) to determine the proportional distribution of the SPM’s prospectus sources. The result shows that the possibility of the source origin of the SPM includes a seagrass fraction (Enhalus acoroides and Thalassia hemprichii), terrestrial C4 plant, macroalgae, and terrestrial C3 plant. The SPM lies between the marine- and terrigenous-end members. However, it seems that the SPM is more to be terrigenous-end and allochthonous. According to a Bayesian mixing model, the terrestrial C4 has the highest contribution of the SPM at all sites except Barugaia and Pasi Island in Selayar (i.e., the highest contribution of the SPM is from the detritus of E. acoroides). The second contribution has been contributed by either seagrass detritus (E. acoroides or Th. hemprichii) or terrestrial C3 plant. The finding of this study indicates that there is a strong influence of the terrigenous sources in the SPM of the seagrass meadows.

suspended particulate matter  /  stable isotope  /  source origin  /  seagrass ecosystems
A’an Johan WAHYUDI, AFDAL. The origin of the suspended particulate matter in the seagrass meadow of tropical waters, an evidence of the stable isotope signatures[J]. Acta Oceanologica Sinica, 2019 , 38 (1) : 136 -143 . DOI: 10.1007/s13131-019-1380-z
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1 Introduction
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Seagrass meadows as a coastal ecosystem play an important role such as organic carbon production and export (due to primary production), nutrient cycling, sediment stabilization, enhanced biodiversity, and trophic transfers to adjacent habitats (Orth et al., 2006). The seagrass meadows altogether with mangrove and coral reef ecosystems provide ecosystem services for the nursery function, e.g., coral reef fishes (Nagelkerken et al., 2000). The seagrass ecosystem is also an important part of global carbon cycles since this ecosystem acts as a carbon sink (Duarte et al., 2013). A seagrass and mangrove ecosystem has been reported to contribute up to 50% top-down carbon sequestration, i.e., 216 Tg/a (Duarte et al., 2004). Furthermore, the global seagrass carbon pool lies up to 8.4 Pg (Fourqurean et al., 2012). Despite its high carbon pool, a seagrass decomposition rate is relatively low. Therefore, the seagrass meadows are potential to be carbon sequester generating surplus of organic carbon production (Duarte et al., 2013) and are crucial for the global carbon cycle (Wahyudi et al., 2016 and references therein).
The carbon cycle in the seagrass meadows is not merely contributed by seagrass species but also by all components such as particulate matter, correspond organisms, chemical and physical factors (Mateo and Romero, 1997; Duarte et al., 2010, 2013; Lavery et al., 2013). Suspended particulate matter (SPM) in the seagrass meadows is expected to have an important contribution in the carbon cycle. As suggested by Kennedy et al. (2010), seagrass vegetation contributes only ~50% carbon burial. The remaning half are contributed by the allochthonous sources such as phytoplankton, marine snow aggregates and terrestrially derived particles (Wahyudi et al., 2016). The important contribution of particulate matter is specifically reported by Wahyudi et al. (2016) that the vertical flux of the aggregates in the seagrass meadows is two orders of magnitude larger than other ecosystems such as coral reef and pelagic.
As previously suggested (e.g., Dalu et al., 2016; Middelburg and Nieuwenhuize, 1998), and according to the result of a marine snow-isotopic profile by Wahyudi et al. (2013), the SPM is not merely composed by a conventional proportional of marine and terrigenous materials. It is expected that the origin/sources of the SPM are either autochthonous or allochthonous. The sources can be from the seagrass detritus, macroalgae, plankton, organisms’ s fecal pellet, sediment, terrestrial plant, and so on (Sarma et al., 2012; Hou et al., 2013). One of the approach to determine the SPM origin is using stable isotope analysis. The stable isotope analysis is a widely used approach in ecology and biogeochemistry, such as determining the food web, diet sources, or the origin of the organic matter pools (Post, 2002; Kennedy et al., 2010; Wahyudi et al., 2013, 2016; Dalu et al., 2016). The use of carbon and nitrogen isotopic-natural-abundance depends on the relative enrichment of 13C and 15N in the organic matter pools (e.g., the SPM in this case) relative to the different sources (Thornton and McManus, 1994; Graham et al., 2001; Dalu et al., 2016).
The study of a SPM’ s isotopic profile is important because the SPM contributes the carbon burial in the seagrass ecosystems (Kennedy et al., 2010; Wahyudi et al., 2016), thus unraveling the origin of the SPM will enhance our knowledge of the proportion of each component that compose the SPM. The evaluation of organic matter contribution to the SPM also provide a baseline assessment of potential diet sources for consumer (Dalu et al., 2016). Since the SPM is expected to be important part of carbon burial, this study will provide the information in carbon sequestration pathways. Furthermore, such kind of study and assessment has not been conducted within Indonesia waters. Thus, we select two study site which represent both pristine (less influenced by anthropogenic activities) and anthropogenic-influenced site. The aim of this study is evaluating the SPM properties that useful to understand the influence factors around the seagrass ecosystem. The objectives of this study are (1) to determine the source of the SPM in the seagrass meadows using natural abundance of carbon and nitrogen stable isotope signature, and (2) to determine the proportions of each prospectus sources of the SPM. By determining the SPM’ s source origin, we expect that the result will be useful to understand the holistic carbon flow in the seagrass ecosystem especially SPM contribution in the carbon sequestration pathways. The SPM’ s source origin can also be used as a good proxy to indicate the stress from terrestrial activities.
2 Materials and methods
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2.1 Field sampling
The sampling was carried out in three locations of the seagrass meadows (Fig. 1), i.e., the coast of Bintan Island, the Selayar Archipelago (Selayar Island and Pasi Island), and Weh Island (Sabang). The first sampling in Bintan was conducted in August 2014, followed by the second sampling in May 2016. The Bintan’ s sites consist of Pengudang, Berakit, Malangrapat and Teluk Bakau. The field sampling in Selayar was conducted in May and August 2015. The Selayar’ s sites consist of Barugaia and Pasi Island. The field sampling in Weh Island (Sabang area) was conducted in May 2016. The methods for collecting marine snow aggregates as explained by Wahyudi et al. (2016) were applied in this research. Water samples were collected in 50 mL of centrifuge tubes. The trap formation sampling followed 2×3 and 3×6 matrix in Bintan and Selayar, respectively. The tissue samples of seagrass were also collected, i.e., the most dominant species, Enhalus acoroides (Ea) and Thalassia hemprichii (Th) during sampling in Bintan Island.
2.2 Stable isotope analysis
The filtrate of the SPM was acidified to remove inorganic carbon using HCl fume for 1 min and neutralized by placing it in a vacuum desiccator with concentrated NaOH for 24 h. The dry weight was measured after oven drying process at 60°C up to constant weight. Each filtrate sample (in glass fiber filter GF/F) was then packed into a tin capsule (Lüdiswiss Sn 98, d 9/10 mm) and stored for further analysis.
The tissue samples of seagrass species were oven-dried at 60°C up to constant weight. The sample was then homogenized using mortar and pestle. About 2–3 mg of homogenized sample was then packed into tin capsule and stored in the vacuum desiccator for further analysis.
The stable isotope analysis was conducted using an isotope ratio mass spectrometer, i.e., thermo delta plus XP coupled to a trace GC ultra with a combi PAL autosampler. The analysis was conducted at the Iso-trace Research, University of Otago (New Zealand).
The stable isotope ratios of 13C/12C and 15N/14N are expressed as δ13C and δ15N, respectively. The isotopic ratios were normalized using Vienna-pee dee belemnite (VPDB) limestone-standard and atmospheric nitrogen (N2). An isotope ratio (R) calculation, given as per-million (‰) deviation from the standard value, was calculated as follows:
$\begin{array}{l}R{ = }^{13}{\rm{C}}{/^{12}}{\rm{C}}\;{\rm{or}}\;R{ = }^{15}{\rm{N}}{/^{14}}{\rm{N}}\\\delta = {\rm{ }}\left[ {\left( {{R_{{\rm{sample}}}}/{R_{{\rm{standard}}}}} \right) - 1} \right]{\rm{ }} \times 1\;000 .\end{array}$
Isotopic and elemental values were determined using laboratory reference materials (USGS-40 and USGS-41). Control materials, namely EDTA-OAS, IAEA-414: algae and IAEA MA-A-1: copepod were used to determine precision and accuracy for Selayar and Bintan samples, respectively. Details information for the stable isotope analysis can be found in, e.g., Carter and Barwick (2011), Lara et al. (2010), Liu et al. (2007a, b), and Wahyudi et al. (2013).
2.3 Determination of proportional distribution
In order to determine the proportional distribution of prospectus sources of the SPM (later the term “source” will be used), we used several secondary data (Table 1). The primary data are the SPM that collected during field sampling. SPM’ s stable isotope values would be the “mixture”.
The proportional contribution of the sources was determined using a hierarchal Bayesian mixing model analysis using MixSIAR (Stock and Semmens, 2013) within 95% credible interval (95% CI). The detail of the analysis was “residual” and “uninformative/generalist” for the error structure and the prior, respectively. The mixing model was run using “long” run length of Markov chain Monte Carlo/MCMC (Stock and Semmens, 2013). Some prospectus sources from secondary data were not included in mixing model analysis after evaluation of the preliminary result of iso-space plot of δ13C against δ15N. The preliminary iso-space plot shows that some of the prospectus sources lie out of the SPM’ s isotopic data range (data not shown). We use discrimination factors namely 1‰ and 1.7‰ for carbon and nitrogen isotopes, respectively. The discrimination factor 1.7‰ for nitrogen was used with the assumption that all the sources and mixture can be categorized as a primary producer (or their proxy). Thus the discrimination factor is half of the discrimination factor from primary producer to the first trophic level which is 3.4‰ (Post, 2002). The MixSIAR’s Bayesian mixing model was performed using R v3.3.1 (http://www.R-project.org/).
3 Results
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The comparison of organic carbon and nitrogen mole ratios (C/N) with carbon and nitrogen isotopes shows the data dispersion of the SPM isotopic and C/N mole ratios values. The minimum C/N mole ratios of the SPM is 9.7 and the maximum value is 25.0. These values lie within the range of marine to terrigenous end-member (Fig. 2). The carbon isotope values ranged from –15.36‰ to –5.15‰ and the nitrogen isotope values ranged from –2.31‰ to 5.54‰. Bi-plot of stable carbon and nitrogen isotopes (Fig. 3) shows that some of the prospectus sources may contribute to the SPM origin. Those sources consist of C4 terrestrial plant, macroalgae, particulate organic matter (POM), and seagrass species (E. acoroides and Th. hemprichii). According to the bi-plot (iso-space plot), the SPM isotopic values distribute scatteringly that show high variability of the source origin.
The stable nitrogen isotope of the SPM shows two groups with distinct differences. About a third of the SPM collected in Bintan have depleted δ15N (negative value), meanwhile almost all of the SPM collected in Selayar have more enriched δ15N (positive value). Almost all depleted δ15N from Bintan were collected in August (during the southwest monsoon). Furthermore, the δ13C values of the SPM collected in Selayar tend to be homogen (lies between –12.00‰ and –2.00‰) compared with the SPM from Bintan which have wider range values.
The iso-space plot of the δ13C againts the δ15N (Fig. 3) shows the possibility of the source origin of the SPM including the seagrass fraction (E. acoroides and Th. hemprichii), terrestrial C4 plant, macroalgae, and terrestrial C3 plant. However, the contribution of each fraction to the mixture cannot be understood merely from the iso-space plot.
The Bayesian mixing model performed using the MixSIAR shows the estimate of the source origin of the SPM (Figs 4 and 5). The statistic summary (data not shown), suggests that according to Figs 4 and 5, the sources origin of the SPM is dominated by the C4 plant followed by the seagrass (E. acoroides) for all sites except for Barugaia, Pasi Island and Sabang. The SPM origin in Barugaia and Pasi Island is dominated by E. acoroides instead. This seagrass species contributes about 24% and 33% in total above- and below-ground habitus for Barugaia, Pasi Island and Sabang, respectively. The C4 plant contributes minimum 8.8% of the total SPM in Sabang (Weh Island) and maximum 64% of total SPM in Berakit. Thalassia hemprichii, as the second dominant species at all sites, contributes 8%–44% of the total SPM, which is comparable with other sources (e.g., macroalgae or POM), except in Sabang that have major contribution. Overall, there is no seasonal variation of the proportional contribution of each source as shown by Fig. 5 (i.e., C4 plant dominant as SPM source followed by E. acoroides). Table 2 shows the highest three contributors of the SPM in the seagrass ecosystem of Bintan, Selayar and Weh Island.
4 Discussion
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The C/N mole ratio of SPM ranged from 9.7 to 25.0. According to Gilhooly et al. (2008) and Martiny et al. (2014), these values lie within the range of marine to terrigenous end-members. Antonio et al. (2012) and Fu et al. (2014) suggested that the C/N mole ratio of SPM which elevated more than 8 indicates the increased-freshwater and/or terrestrial sources contributions. Either Antonio et al. (2012) or Fu et al. (2014) assessed the SPM in estuaries. Thus cannot be compared directly with the seagrass ecosystem’ s SPM in the present study. However, according to the evaluation by comparing the present study with the study by Antonio et al. (2012) or Fu et al. (2014), it is clear that the SPM in the present study tends to be terrigenous by means the increased terrestrial sources contributions.
It has been expected that the stable carbon and nitrogen isotope values show high variability, since the SPM composed by many sources/materials. As suggested by Sarma et al. (2012) and Hou et al. (2013), the sources can be from the seagrass detritus, macroalgae, plankton, organisms’ s fecal pellet, sediment, terrestrial plant, and so on. Wahyudi et al. (2016) also explained that the marine snow (another typical name of the SPM) is composed by the POM, mesograzer fecal pellet and seagrass detritus. Therefore, the wide range SPM’s isotopic values indicate the different major compositions of each SPM sample.
A mixing model shows that the sources origin of the SPM is dominated by the C4 plant followed by the seagrass (E. acoroides) for all sites in Bintan. Meanwhile, the SPM in Selayar’ s seagrass meadows that represent by sites in Barugaia and Pasi Island, is dominated by the seagrass detritus (E. acoroides). The SPM in Sabang is dominated by Th. hemprichii detritus (Fig. 4). The seagrass meadows in Selayar can be categorized more pristine ecosystem compared with those in Bintan (unpublished data). This may affect the composition of the SPM in both areas, Bintan and Selayar. The C4 plant that dominates the SPM composition in Bintan may be caused by the high amount of the terrestrial loading, i.e., detritus export from terrestrial plantations or grassland to the coastal ecosystem. This finding suggests that the SPM in the seagrass meadows that located in island with high anthropogenic stress (i.e., land use change) will be likely composed mainly by terrigenous materials.
On the contrary, the seagrass meadows of Pasi Island and Barugaia in Selayar and also Sabang shows different SPM profiles. The stable isotope profile of the SPM shows the dominance of the seagrass detritus (i.e., E. acoroides) on the SPM composition. Another autochthonous source of the SPM, e.g., Th. hamprichii, has medium proportions (except for Sabang which is majority), since this species is the second dominant species following E. acoroides.
This study suggests that there is no different trends obtained in May and August. However, there is still no data obtained from the periods of October to March. Therefore, we expect there is still a minor or insignificant differences due to the seasonal changes. Previous studies of the seagrass ecosystem, suggested that there are seasonal variabilities of the net productivity in the seagrass meadows caused by physical factors such as temperature and light (Herzka and Dunton, 1997), environmental stress (Carr et al., 2012), or anthropogenic activities (Fourqurean et al., 2001). The seasonal variability of the seagrass production may affect the detritus production that contribute to the SPM composition. Furthermore, an SPM concentration may be changes seasonally, as suggested by Mityaev and Berger (2014), mainly due to abiotic factors such as water temperature and tide events. Although our result shows the similar SPM composition indifferent seasons, the possibility of the seasonal changes in the SPM composition should be evaluated for the future direction of SPM studies.
Kennedy et al. (2010) suggested that the seagrass vegetation contributes only ~50% carbon burial in the sediment. We can assume that the other half are contributed by the other sources, such as detritus, fecal pellet, planktonic organisms, marine snow aggregates or particulate matter. Wahyudi et al. (2016) suggested that the particulate matter can be exported downward to the sediment as much as 5.4 kt/a C within 964.2 hm2 seagrass meadows. This value is equal to 5.6 t/(hm2∙a). Altogether with the seagrass detritus, the particulate matter can be deposited or buried in the bottom of the seagrass meadows. This process can be distinguished as the contribution in the carbon sequestration. However, as mentioned by Wahyudi et al. (2016) there is a dissonance in the estimation of the vertical flux of the SPM (or marine snow aggregates) compared with the carbon storage capacity in the seagrass meadows. Duarte et al. (2013) also explained that only half of the seagrass net production are buried downward. Therefore, in order to determine the exact SPM contribution in the carbon sequestration, we need to know the fate of the SPM after exported downward. One of the key process that can be assessed is the decomposition rate of the SPM in both water column and bottom of the seagrass meadows.
5 Conclusions
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The SPM lies between the marine- and terrigenous-end member but tends to be be terrigenous and allochthonous. The terrestrial C4 plant has the highest contribution of the SPM at all sites of Bintan. The highest contribution of SPM in Barugaia and Pasi Island is from the detritus of E. acoroides. The second contribution has been made by either seagrass detritus (E. acoroides or Th. hemprichii), terrestrial C3 plant or even soil materials. There is no different trends obtained in the different time periods (May and August). Our finding indicates that there is a strong influence of the terrestrial sources in the SPM of seagrass meadows. However, the influences seem to be site specific. The seagrass contribution would be the highest at pristine seagrass meadows (e.g., Pasi Island) compared with the disrupted areas (e.g., east coast of Bintan).
Acknowledgements
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The field and laboratory assistance by Madisaeni and Suci Lastrini is well acknowledged. The English guidance from Supono is also highly appreciated.
Funding
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  • The Core Competence Research Project 2014; the Research Agenda COREMAP-CTI 2015-2016; the “Unggulan LIPI” Research Project 2017.
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doi: 10.1007/s13131-019-1380-z
  • Receive Date：2017-11-27
  • Online Date：2026-03-31
  • Published：2019-01-25
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  • Received：2017-11-27
  • Accepted：2018-04-20
Funding
The Core Competence Research Project 2014; the Research Agenda COREMAP-CTI 2015-2016; the “Unggulan LIPI” Research Project 2017.
Affiliations
    1 Research Center for Oceanography, Indonesian Institute of Sciences, Jakarta 14430, Indonesia

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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