Skip to main content

Advertisement

SpringerLink
Log in

Carbon Sources of Sediment and Epifaunal Food Sources in a Tropical Mangrove Forest in North Sulawesi, Indonesia

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

The stable isotope ratios of nitrogen (δ15N) and carbon (δ13C) were applied in this study to analyze sediment carbon sources and primary food sources of epifauna in an oceanic mangrove forest in tropical North Sulawesi, Indonesia. Proportional contribution of mangrove-derived carbon to the food sources was compared among epifauna belonging to different feeding guilds. The sediment in the mangrove site with a depleted δ13C signature (−28.02‰±0.24‰) mainly consists of mangrove-derived carbon. Analysis using Bayesian stable isotope mixing model in the R program shows that mangrove-derived carbon can dominate the food sources of a majority of the epifauna (11 out of the total 18 species), especially 2 sesarmid crabs Parasesarma semperi and Sesarma sp., crab Epixanthus dentatus, and snails Terebralia sulcata and Optediceros breviculum, which belong to various feeding guilds. Mangrove-derived carbon has a proportional contribution to the food sources of fiddle crab Tubuca coarctata and 3 littorinid snails (Littoraria spp.) close to that of suspended particulate organic matter. Three planktophagous bivalve species (Anadara antiquata, Anadara sp. and Callista erycina) were found to mainly feed on seagrass-derived materials. Mean proportional contributions of mangrove-derived carbon to the food sources were 50.15%, 59.60%, 46.20% and 27.58% for the carnivorous, omnivorous, phytophagous and planktophagous groups, respectively. The results suggest that mangrove-derived carbon can directly (via grazing plant tissues) or indirectly (via deposit feedings) make an important contribution to the food sources of epifauna in the oceanic mangrove forest where the allochthonous input of organic carbon is low.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abrantes, K. G., Johnston, R., Connolly, R. M., and Sheaves, M., 2015. Importance of mangrove carbon for aquatic food webs in wet-dry tropical estuaries. Estuaries and Coasts, 38 (1): 383–399, DOI: https://doi.org/10.1007/s12237-014-9817-2.

    Google Scholar 

  • Alfaro, A. C., 2008. Diet of Littoraria scabra, while vertically migrating on mangrove trees: Gut content, fatty acid, and stable isotope analyses. Estuarine, Coastal and Shelf Science, 79 (4): 718–726, DOI: https://doi.org/10.1016/j.ecss.2008.06.016.

    Google Scholar 

  • Al-Maslamani, I., Walton, M. E. M., Kennedy, H. A., Al-Mohannadi, M., and Le Vay, L., 2013. Are mangroves in arid environments isolated systems? Life-history and evidence of dietary contribution from inwelling in a mangrove-resident shrimp species. Estuarine, Coastal and Shelf Science, 124: 56–63, DOI: https://doi.org/10.1016/j.ecss.2013.03.007.

    Google Scholar 

  • Alongi, D. M., 2009. The Energetics of Mangrove Forests. Springer Verlag, Dordrecht, 216pp.

    Google Scholar 

  • Bouillon, S., Koedam, N., Raman, A. V, and Dehairs, F., 2002. Primary producers sustaining macro-invertebrate communities in intertidal mangrove forests. Oecologia, 130 (3): 441–448, DOI: https://doi.org/10.1007/s004420100814.

    Google Scholar 

  • Bouillon, S., Moens, T., Overmeer, I., Koedam, N., and Dehairs, F., 2004. Resource utilization patterns of epifauna from mangrove forests with contrasting inputs of local versus imported organic matter. Marine Ecology Progress Series, 278: 77–88, DOI: https://doi.org/10.3354/meps278077.

    Google Scholar 

  • Chen, G, Azkab, M. H., Chmura, G, Chen, S., Sastrosuwondo, P., Ma, Z., Dharmawan, I. W. E., Yin, X., and Chen, B., 2017. Mangroves as a major source of soil carbon storage in adjacent seagrass meadows. Scientific Reports, 7 (1): 42406, DOI: https://doi.org/10.1038/srep42406.

    Google Scholar 

  • Chen, G., Chen, B., Yu, D., Tam, N. F. Y., Ye, Y., and Chen, S., 2016. Soil greenhouse gas emissions reduce the contribution of mangrove plants to the atmospheric cooling effect. Environmental Research Letters, 11 (12): 124019, DOI: https://doi.org/10.1088/1748-9326/11/12/124019.

    Google Scholar 

  • Chen, G., Yu, D., Ye, Y., and Chen, B., 2013. Impacts of mangrove vegetation on macro-benthic faunal communities. Acta Ecologica Sinica, 33 (2): 327–366, DOI: https://doi.org/10.5846/stxb201111091699 (in Chinese with English abstract).

    Google Scholar 

  • Chen, S., Chen, B., Sastrosuwondo, P., Dharmawan, I. W. E., Ou, D., Yin, X., Yu, W., and Chen, G., 2018. Ecosystem carbon stock of a tropical mangrove forest in North Sulawesi, Indonesia. Acta Oceanologica Sinica, 37 (12): 85–91, DOI: https://doi.org/10.1007/s13131-018-1290-5.

    Google Scholar 

  • Chen, S., Chen, G., Chen, B., Ye, Y., and Ma, Z., 2014. Feeding ecology of sesarmid crabs in mangroves. Acta Ecologica Sinica, 34 (19): 5349–5359, DOI: https://doi.org/10.5846/stxb201301160110 (in Chinese with English abstract).

    Google Scholar 

  • Chong, V. C., Low, C. B., and Ichikawa, T., 2001. Contribution of mangrove detritus to juvenile prawn nutrition: A dual stable isotope study in a Malaysian mangrove forest. Marine Biology, 138 (1): 77–86, DOI: https://doi.org/10.1007/s002270000434.

    Google Scholar 

  • Connolly, R. M., Gorman, D., and Guest, M. A., 2005. Movement of carbon among estuarine habitats and its assimilation by invertebrates. Oecologia, 144 (4): 684–691, DOI: https://doi.org/10.1007/s00442-005-0167-4.

    Google Scholar 

  • Gao, X., Wang, M., Wu, H., Wang, W., and Tu, Z., 2018. Effects of Spartina alterniflora invasion on the diet of mangrove crabs (Parasesarma plicata) in the Zhangjiang Estuary, China. Journal of Coastal Research, 34 (1): 106–113, DOI: https://doi.org/10.2112/JCOASTRES-D-17-00002.1.

    Google Scholar 

  • Giarrizzo, T., Schwamborn, R., and Saint-Paul, U., 2011. Utilization of carbon sources in a northern Brazilian mangrove ecosystem. Estuarine, Coastal and Shelf Science, 95 (4): 447–457, DOI: https://doi.org/10.1016/j.ecss.2011.10.018.

    Google Scholar 

  • Giri, C., Ochieng, E., Tieszen, L. L., Zhu, Z., Singh, A., Loveland, T., Masek, J., and Duke, N., 2011. Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecology and Biogeography, 20 (1): 154–159, DOI: https://doi.org/10.1111/j.1466-8238.2010.00584.x.

    Google Scholar 

  • Hsieh, H. L., Chen, C. P., Chen, Y. G., and Yang, H. H., 2002. Diversity of benthic organic matter flows through polychaetes and crabs in a mangrove estuary: δ13C and δ34S signals. Marine Ecology Progress Series, 227: 145–155.

    Google Scholar 

  • Jennerjahn, T. C., and Ittekkot, V, 2002. Relevance of mangroves for the production and deposition of organic matter along tropical continental margins. Naturwissenschaften, 89 (1): 23–30, DOI: https://doi.org/10.1007/s00114-001-0283-x.

    Google Scholar 

  • Kieckbusch, D. K., Koch, M. S., Serafy, J. E., and Anderson, W. T., 2004. Trophic linkages among primary producers and consumers in fringing mangroves of subtropical lagoons. Bulletin of Marine Science, 74 (2): 271–285.

    Google Scholar 

  • Kon, K., Kawakubo, N., Aoki, J. I., Tongnunui, P., Hayashizaki, K. I., and Kurokura, H., 2009. Effect of shrimp farming organic waste on food availability for deposit feeder crabs in a mangrove estuary, based on stable isotope analysis. Fisheries Science, 75 (3): 715–722, DOI: https://doi.org/10.1007/s12562-009-0060-x.

    Google Scholar 

  • Kristensen, D. K., Kristensen, E., and Mangion, P., 2010. Food partitioning of leaf-eating mangrove crabs (Sesarminae): Experimental and stable isotope (δ13C and δ15N) evidence. Estuarine, Coastal and Shelf Science, 87 (4): 583–590, DOI: https://doi.org/10.1016/j.ecss.2010.02.016.

    Google Scholar 

  • Lai, T., and He, B., 1998. Studies on the macrobenthos species diversity for Guangxi mangrove areas. Guangxi Science, 5 (03): 7–13, DOI: https://doi.org/10.13656/j.cnki.gxkx.1998.03.002 (in Chinese with English abstract).

    Google Scholar 

  • Le, Q. D., Haron, N. A., Tanaka, K., Ishida, A., Sano, Y., Dung, L. V., and Shirai, K., 2017. Quantitative contribution of primary food sources for a mangrove food web in Setiu lagoon from east coast of Peninsular Malaysia, stable isotopic (δ13C and δ15N) approach. Regional Studies in Marine Science, 9: 174–179, DOI: https://doi.org/10.1016/j.rsma.2016.12.013.

    Google Scholar 

  • Lee, O. H. K., Williams, G. A., and Hyde, K. D., 2001. The diets of Littoraria ardouiniana and L. melanostoma in Hong Kong mangroves. Journal of the Marine Biological Association of the United Kingdom, 81 (6): 967–973, DOI: https://doi.org/10.1017/S002531540100491X.

    Google Scholar 

  • Lee, S. Y., 1997. Potential trophic importance of the faecal material of the mangrove sesarmine crab Sesarma messa. Marine Ecology Progress Series, 159: 275–284, DOI: https://doi.org/10.3354/meps159275.

    Google Scholar 

  • Lin, J., Huang, Y., Arbi, U. Y., Lin, H., Azkab, M. H., Wang, J., He, X., Mou, J., Liu, K., and Zhang, S., 2018. An ecological survey of the abundance and diversity of benthic macrofauna in Indonesian multispecific seagrass beds. Acta Oceanologica Sinica, 37 (6): 82–89, DOI: https://doi.org/10.1007/s13131-018-1181-9.

    Google Scholar 

  • Macintosh, D., 1980. Ecology and productivity of Malaysian mangrove crab populations (Decapoda: Brachyura). The Asian Symposium on Mangrove Environment. Kuala Lumpur, 354–377.

  • Mccutchan, J. H., Lewis, W. M., Kendall, C., and Mcgrath, C. C., 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos, 102 (2): 378–390.

    Google Scholar 

  • Meziane, T., and Tsuchiya, M., 2002. Organic matter in a subtropical mangrove-estuary subjected to wastewater discharge: Origin and utilisation by two macrozoobenthic species. Journal of Sea Research, 47 (1): 1–11, DOI: https://doi.org/10.1016/S1385-1101(01)00092-2.

    Google Scholar 

  • Murdiyarso, D., Purbopuspito, J., Kauffman, J. B., and Mcgrath, C. C., 2015. The potential of Indonesian mangrove forests for global climate change mitigation. Nature Climate Change, 5 (12): 1089–1092, DOI: https://doi.org/10.1038/nclimate2734.

    Google Scholar 

  • Newell, R. I. E., Marshall, N., Sasekumar, A., and Chong, V. C., 1995. Relative importance of benthic microalgae, phytoplankton, and mangroves as sources of nutrition for penaeid prawns and other coastal invertebrates from Malaysia. Marine Biology, 123 (3): 595–606, DOI: https://doi.org/10.1007/BF00349238.

    Google Scholar 

  • Park, H. J., Park, T. H., Kang, C. K., and Kang, H. Y., 2017. Comparative trophic structures of macrobenthic food web in two macrotidal wetlands with and without a dike on the temperate coast of Korea as revealed by stable isotopes. Marine Environmental Research, 131: 134–145, DOI: https://doi.org/10.1016/j.marenvres.2017.09.018.

    Google Scholar 

  • Poon, D. Y. N., Chan, B. K. K., and Williams, G. A., 2010. Spatial and temporal variation in diets of the crabs Metopograpsus frontalis (Grapsidae) and Perisesarma bidens (Sesarmidae): Implications for mangrove food webs. Hydrobiologia, 638 (1): 29–40, DOI: https://doi.org/10.1007/s10750-009-0005-5.

    Google Scholar 

  • Quan, W., Ying, M., Zhou, Q., and Xu, C., 2018. Carbon source analysis of bivalve-culture based on stable carbon isotope technique. Journal of Shanghai Ocean University, 27 (2): 175–180 (in Chinese with English abstract).

    Google Scholar 

  • Ranjan, R. K., Routh, J., Ramanathan, A. L., and Klump, J. V., 2011. Elemental and stable isotope records of organic matter input and its fate in the Pichavaram mangrove-estuarine sediments (Tamil Nadu, India). Marine Chemistry, 126 (1): 163–172, DOI: https://doi.org/10.1016/j.marchem.2011.05.005.

    Google Scholar 

  • Rodelli, M. R., Gearing, J. N., Gearing, P. J., Marshall, N., and Sasekumar, A., 1984. Stable isotope ratio as a tracer of mangrove carbon in Malaysian ecosystems. Oecologia, 61 (3): 326–333, DOI: https://doi.org/10.1007/BF00379629.

    Google Scholar 

  • Sprintall, J., Potemra, J. T., Hautala, S. L., Bray, N. A., and Pandoe, W. W., 2003. Temperature and salinity variability in the exit passages of the Indonesian Throughflow. Deep-Sea Research Part II, 50 (12): 2183–2204, DOI: https://doi.org/10.1016/S0967-0645(03)00052-3.

    Google Scholar 

  • Thimdee, W., Deein, G., Sangrungruang, C., and Matsunaga, K., 2004. Analysis of primary food sources and trophic relationships of aquatic animals in a mangrove-fringed estuary, Khung Krabaen Bay (Thailand) using dual stable isotope techniques. Wetlands Ecology and Management, 12 (2): 135–144, DOI: https://doi.org/10.1023/b:wetl.0000021674.76171.69.

    Google Scholar 

  • Thongtham, N., and Kristensen, E., 2005. Carbon and nitrogen balance of leaf-eating sesarmid crabs (Neoepisesarma versicolor) offered different food sources. Estuarine, Coastal and Shelf Science, 65 (1): 213–222, DOI: https://doi.org/10.1016/j.ecss.2005.05.014.

    Google Scholar 

  • Tue, N. T., Hamaoka, H., Sogabe, A., Quy, T. D., Nhuan, M. T., and Omori, K., 2012. Food sources of macro-invertebrates in an important mangrove ecosystem of Vietnam determined by dual stable isotope signatures. Journal of Sea Research, 72: 14–21, DOI: https://doi.org/10.1016/j.seares.2012.05.006.

    Google Scholar 

  • Vannini, M., Cannicci, S., and Fratini, S., 2001. Prey selection of Epixanthus dentatus (Crustacea: Brachyura: Eriphiidae) as determined by its prey remains. Journal of the Marine Biological Association of the United Kingdom, 81 (3): 455–459, DOI: https://doi.org/10.1017/S0025315401004088.

    Google Scholar 

  • Xue, B., Yan, C., Lu, H., and Bai, Y., 2009. Mangrove-derived organic carbon in sediment from Zhangjiang Estuary (China) mangrove wetland. Journal of Coastal Research, 25 (4): 949–956, DOI: https://doi.org/10.2112/08-1047.1.

    Google Scholar 

  • Yang, M., Gao, T., Xing, Y, Yu, Z., Ying, N., and Wen, A., 2017. Study on the food sources of mangrove macrobenthos in Lianzhou Bay. Guangxi Sciences, 24 (5): 490–497, DOI: https://doi.org/10.13656/j.cnki.gxkx.20170920.001 (in Chinese with English abstract).

    Google Scholar 

  • Yu, J., Chen, P. M., and Feng, X., 2016. Food habits and trophic levels for 4 species of economical shrimps in the Pearl River Estuary shallow waters. Journal of Southern Agriculture, 47 (5): 736–741 (in Chinese with English abstract).

    Google Scholar 

  • Zou, L., Yao, X., Yamaguchi, H., Guo, X., Gao, H., Wang, K., and Sun, M., 2018. Seasonal and spatial variations of macro benthos in the intertidal mudflat of southern Yellow River Delta, China in 2007/2008. Journal of Ocean University of China, 17 (2): 437–444, DOI: https://doi.org/10.1007/s11802-018-3313-4.

    Google Scholar 

Download references

Acknowledgements

This study was supported by the National Key Technologies Research and Development Program of China (No. 2017YFC0506101), the China-ASEAN Maritime Fund ‘Monitoring and Conservation of the Coastal Ecosystems in the South China Sea’, and the National Natural Science Foundation of China (No. 31101876). The authors are grateful to Mr. Asep Rasyidin, Mr. Mochtar Djabar and Dr. Xijie Yin for their assistance with field sampling and laboratory analysis.

Author information

Authors and Affiliations

  1. College of Marine Life Sciences, Ocean University of China, Qingdao, 266000, China

    Zhiqiang Wu & Limei Xie

  2. Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, 361005, China

    Limei Xie, Bin Chen, Shunyang Chen & Guangcheng Chen

  3. Research Center for Oceanography, Indonesian Institute of Sciences, Jakarta, 11048, Indonesia

    I. Wayan Eka Dhamawan, Pramudji Sastrosuwondo, Pratiwi Rianta & Widyastuti Ernawati

  4. Observation and Research Station of Coastal Wetland Ecosystem in Beibu Bay, Ministry of Natural Resources, Beihai, 536015, China

    Shunyang Chen & Guangcheng Chen

Authors
  1. Zhiqiang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Limei Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. Wayan Eka Dhamawan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pramudji Sastrosuwondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shunyang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pratiwi Rianta
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Widyastuti Ernawati
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Guangcheng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guangcheng Chen.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Z., Xie, L., Chen, B. et al. Carbon Sources of Sediment and Epifaunal Food Sources in a Tropical Mangrove Forest in North Sulawesi, Indonesia. J. Ocean Univ. China 19, 1169–1176 (2020). https://doi.org/10.1007/s11802-020-4401-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-020-4401-9

Key words

Search

Navigation