Estuaries and Coasts

, Volume 40, Issue 5, pp 1437–1449 | Cite as

Nematode Responses to the Invasion of Exotic Spartina in Mangrove Wetlands in Southern China

  • Sujing Fu
  • Lizhe CaiEmail author
  • Jing Cao
  • Xinwei Chen


Investigations into nematode density and species assemblages have been conducted in different types of mangroves worldwide, but these studies have typically been limited to one type of plant or tree species. The invasive salt marsh grass Spartina alterniflora has successively invaded native mangroves along the southern coasts of China during the preceding two decades. However, few meiofauna studies on the impacts of S. alterniflora have been conducted, and the consequences of this invasion on ecosystem composition and function remain unclear. The hypothesis of this study was that the spatial and seasonal distribution of nematode assemblages vary significantly among three native mangrove habitats (Kandelia obovata, Aegiceras corniculatum, and Avicennia marina) and between these habitats and a fourth habitat that was colonized by S. alterniflora, in Zhangjiang Estuary, China. Our results demonstrated that different species dominated in different habitats seasonally. Highly significant differences in density, number of species, diversity index, and maturity index were present among the four habitats. ANOSIM results revealed that there were significant differences in nematode assemblages among the four habitats and seasons, with the S. alterniflora habitat exhibiting the lowest mean values of number of species, Shannon-Wiener diversity index, richness index, and maturity index in the four seasons. This suggests that the presence of S. alterniflora disrupted nematode assemblages.


Mangrove Spartina alterniflora Marine nematodes Zhangjiang Estuary 



This study was financed by the National Natural Science Foundation of China (41376113) and public science and technology research funds for marine projects (201505004). Dr. Guy Boucher of Muséum National d’Histoire Naturelle, Paris, Dr. Hans-U. Dahms of Kaohsiung Medical University, Dr. Stephen C. Landers of Troy University, and Dr. Enming He of Fujian Institute of Subtropical Botany are thanked for their valuable comments on earlier versions of the manuscript. We are grateful to Sha Liu, Peng Xu, Xin Peng, and Chen Wu for their assistance in field sampling and to Jiemin Guo for providing environmental data. We also sincerely thank the anonymous reviewers for scientific comments and valuable suggestions.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.


  1. Alongi, D.M. 1987a. Inter-estuary variation and intertidal zonation of free-living nematode communities in tropical mangrove systems. Marine Ecology Progress Series 40: 103–114.CrossRefGoogle Scholar
  2. Alongi, D.M. 1987b. The influence of mangrove-derived tannins on intertidal meiobenthos in tropical estuaries. Oecologia 71: 537–540.CrossRefGoogle Scholar
  3. Alongi, D.M. 2002. Present state and future of the world’s mangrove forests. Environmental Conservation 29: 331–349.CrossRefGoogle Scholar
  4. Ansari, K.G.M.T., S. Manokaran, S. Raja, P.S. Lyla, and S. Ajmal-Khan. 2014. Interaction of free-living marine nematodes in the artificial mangrove environment (southeast coast of India). Environmental Monitoring and Assessment 186: 293–305.CrossRefGoogle Scholar
  5. Armenteros, M., I. Martín, J.P. Williams, B. Creagh, G. González-Sansón, and N. Gapetillo. 2006. Spatial and temporal variations of meiofaunal communities from the western sector of the Gulf of Batabanó, Cuba. Estuaries and Coasts 29: 124–132.CrossRefGoogle Scholar
  6. Austen, M.C., and R.M. Warwick. 1989. Comparison of univariate and multivariate aspects of estuarine meiobenthic community structure. Estuarine Coastal and Shelf Science 29: 23–42.CrossRefGoogle Scholar
  7. Balsamo, M., G. Albertelli, V.U. Ceccherelli, R. Coccioni, M.A. Colangelo, M. Curini-Galletti, R. Danovaro, R. D’Addabbo, C. De Leonardis, M. Fabiano, F. Frontalini, M. Gallo, C. Gambi, L. Guidi, M. Moreno, A. Pusceddu, R. Sandulli, F. Semprucci, M.A. Todaro, and P. Tongiorgi. 2010. Meiofauna of the Adriatic Sea: present knowledge and future perspectives. Chemistry and Ecology 26: 45–63.CrossRefGoogle Scholar
  8. Balsamo, M., F. Semprucci, F. Frontalini, and R. Coccioni. 2012. Meiofauna as a tool for marine ecosystem biomonitoring. In Marine ecosystems, ed. A. Cruzado, vol. 4, 77–104. Rijeka: InTech Publisher.Google Scholar
  9. Bongers, T. 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83: 14–19.CrossRefGoogle Scholar
  10. Bongers, T., R. Alkemade, and G.W. Yeates. 1991. Interpretation of disturbance-induced maturity decrease in marine nematode assemblages by means of the maturity index. Marine Ecology Progress Series 76: 135–142.CrossRefGoogle Scholar
  11. Chang, Y., and Y.Q. Guo. 2014. Study on meiofauna abundance and nematode diversity in mangrove of Luoyang river, Fujian province. Journal of Jimei University (Natural Science) 19: 7–12 [In Chinese with English abstract].Google Scholar
  12. Chen, G.C., and Y. Ye. 2008. Leaf consumption by Sesarma plicata in a mangrove forest at Jiulongjiang estuary, China. Marine Biology 154: 997–1007.CrossRefGoogle Scholar
  13. Chen, H.L., B. Li, C.M. Fang, J.K. Chen, and J.H. Wu. 2007a. Exotic plant influences soil nematode communities through litter input. Soil Biology & Biochemistry 39: 1782–1793.CrossRefGoogle Scholar
  14. Chen, H.L., B. Li, J.B. Hu, J.K. Chen, and J.H. Wu. 2007b. Effects of Spartina alterniflora invasion on benthic nematode communities in the Yangtze estuary. Marine Ecology Progress Series 336: 99–110.CrossRefGoogle Scholar
  15. Chen, L.Z., W.Q. Wang, Y.H. Zhang, and G.H. Lin. 2009. Recent progresses in mangrove conservation, restoration and research in China. Journal of Plant Ecology 2: 45–54.CrossRefGoogle Scholar
  16. Chinnadurai, G., and O.J. Fernando. 2007. Meiofauna of mangroves of the southeast coast of India with special reference to the free-living marine nematode assemblage. Estuarine Coastal and Shelf Science 72: 329–336.CrossRefGoogle Scholar
  17. Clarke, K.R., and R.M. Warwick. 2001. Change in marine communities: an approach to statistical analysis and interpretation. Google Scholar
  18. Coull, B.C. 1999. Role of meiofauna in estuarine soft-bottom habitats. Australian Journal of Ecology 24: 327–343.CrossRefGoogle Scholar
  19. Duke, N.C. 1991. A systematic revision of the mangrove genus Avicennia (Avicenniaceae) in Australasia. Australian Systematic Botany 4: 299–324.CrossRefGoogle Scholar
  20. Dye, A.H. 2006. Persistent effects of physical disturbance on meiobenthos in mangrove sediments. Marine Environmental Research 62: 341–355.CrossRefGoogle Scholar
  21. Ge, B.M., Y.X. Bao, H.Y. Cheng, D.Z. Zhang, and Z.Y. Hu. 2012. Influence of Spartina alterniflora invasion stages on macrobenthic communities on a tidal flat in Wenzhou Bay, China. Brazilian Journal of Oceanography 60: 441–448.CrossRefGoogle Scholar
  22. Gee, J.M., and P.J. Somerfield. 1997. Do mangrove diversity and leaf litter decay promote meiofaunal diversity? Journal of Experimental Marine Biology and Ecology 218: 13–33.CrossRefGoogle Scholar
  23. Giere, O. 1993. Meiobenthology. The microscopic fauna in aquatic sediments. Berlin: Springer-Verlag.Google Scholar
  24. Gingold, R., M. Mundo-Ocampo, O. Holovachov, and A. Rocha-Olivares. 2010. The role of habitat heterogeneity in structuring the community of intertidal free-living marine nematodes. Marine Biology 157: 1741–1753.CrossRefGoogle Scholar
  25. Guilini, K., T.N. Bezerra, T. Deprez, G. Fonseca, O. Holovachov, D. Leduc, D. Miljutin, T. Moens, J. Sharma, N. Smol, A. Tchesunov, V. Mokievsky, J. Vanaverbeke, A. Vanreusel, and M. Vincx. 2016. NeMys: World Database of Free-Living Marine Nematodes. on 2016–06-20.
  26. Guo, Y.Q. 2008. The study on the community of free-living marine nematodes in Fenglin mangrove wetlands, Xiamen, China. Acta Oceanologica Sinica 30: 147–153 [In Chinese with English abstract].Google Scholar
  27. Gwyther, J. 2003. Nematode assemblages from Avicennia marina leaf litter in a temperate mangrove forest in South-Eastern Australia. Marine Biology 142: 289–297.CrossRefGoogle Scholar
  28. Hedge, P., and L. Kriwoken. 2000. Evidence for effects of Spartina anglica invasion on benthic macrofauna in little Swanport estuary, Tasmania. Austral Ecology 25: 150–159.CrossRefGoogle Scholar
  29. Heip, C., M. Vincx, and G. Vranken. 1985. The ecology of marine nematodes. Oceanographic Marine Biology Annual Review 23: 399–489.Google Scholar
  30. Hourston, M., I.C. Potter, R.M. Warwick, F.J. Valesini, and K.R. Clarke. 2009. Spatial and seasonal variations in the ecological characteristics of the free-living nematode assemblages in a large microtidal estuary. Estuarine Coastal and Shelf Science 82: 309–322.CrossRefGoogle Scholar
  31. Kennedy, A.D. 1994. Carbon partitioning within meiobenthic nematode communities in the exe estuary, UK. Marine Ecology Progress Series 105: 71–78.CrossRefGoogle Scholar
  32. Lee, H.Y., and S.S. Shih. 2004. Impacts of vegetation changes on the hydraulic and sediment transport characteristics in Guandu mangrove wetland. Ecological Engineering 23: 85–94.CrossRefGoogle Scholar
  33. Lin, P. 1999. Mangrove ecosystem in China. Beijing: Science Press.Google Scholar
  34. Liu, J.C., C.L. Yan, and M.R. Macnair. 2006. Distribution and speciation of some metals in mangrove sediments from Jiulong River estuary, People’s Republic of China. Bulletin of Environmental Contamination and Toxicology 76: 815–822.CrossRefGoogle Scholar
  35. Liu, J.C., C.L. Yan, L.S. Kate, R.F. Zhang, and H.L. Lu. 2010. The distribution of acid-volatile sulfide and simultaneously extracted metals in sediments from a mangrove forest and adjacent mudflat in Zhangjiang estuary, China. Marine Pollution Bulletin 60: 1209–1216.CrossRefGoogle Scholar
  36. Liu, J.L., B. Huang, and Z.W. Liang. 2013. Study on abundance and biomass of benthic meiofauna in mangrove of Dongzhai Bay. Acta Oceanologica Sinica 35: 187–192 [In Chinese with English abstract].Google Scholar
  37. Merckx, B., P. Goethals, M. Steyaert, A. Vanreusel, M. Vincx, and J. Vanaverbeke. 2009. Predictability of marine nematode biodiversity. Ecological Modelling 220: 1449–1458.CrossRefGoogle Scholar
  38. Mokievsky, V.O., A.V. Tchesunov, A.A. Udalov, and N.D. Toan. 2011. Quantitative distribution of meiobenthos and the structure of the free-living nematode community of the mangrove intertidal zone in Nha Trang Bay (Vietnam) in the South China Sea. Russian Journal of Marine Biology 37: 272–283.CrossRefGoogle Scholar
  39. Moreno, M., T.J. Ferrero, I. Gallizia, L. Vezzulli, G. Albertelli, and M. Fabiano. 2008. An assessment of the spatial heterogeneity of environmental disturbance within an enclosed harbour through the analysis of meiofauna and nematode assemblages. Estuarine Coastal and Shelf Science 77: 565–576.CrossRefGoogle Scholar
  40. Moreno, M., F. Semprucci, L. Vezzulli, M. Balsamo, M. Fabiano, and G. Albertelli. 2011. The use of nematodes in assessing ecological quality status in the Mediterranean coastal ecosystems. Ecological Indicators 11: 328–336.CrossRefGoogle Scholar
  41. Ndaro, S.G.M., and E. Ólafsson. 1999. Soft-bottom fauna with emphasis on nematode assemblage structure in a tropical intertidal lagoon in Zanzibar, eastern Africa: I. Spatial variability. Hydrobiologia 405: 133–148.CrossRefGoogle Scholar
  42. Netto, S.A., and F. Gallucci. 2003. Meiofauna and macrofauna communities in a mangrove from the island of Santa Catarina, South Brazil. Hydrobiologia 505: 159–170.CrossRefGoogle Scholar
  43. Nicholas, W.L., J.A. Elek, A.C. Stewart, and T.G. Marples. 1991. The nematode fauna of a temperate Australian mangrove mudflat; its population density, diversity and distribution. Hydrobiologia 209: 13–27.CrossRefGoogle Scholar
  44. Nicholas, W.L., and A.C. Stewart. 1993. The nematode fauna of two estuarine mangrove mud-flats on the south coast of new South Wales. Wetlands (Australia) 12: 16–28.Google Scholar
  45. Ólafsson, E., S. Carlström, and S.G.M. Ndaro. 2000. Meiobenthos of hypersaline tropical mangrove sediment in relation to spring tide inundation. Hydrobiologia 426: 57–64.CrossRefGoogle Scholar
  46. Osenga, G.A., and B.C. Coull. 1983. Spartina alterniflora Loisel root structure and meiofaunal abundance. Journal of Experimental Marine Biology and Ecology 67: 221–225.CrossRefGoogle Scholar
  47. Pinto, T.K., M.C.V. Austen, R.M. Warwick, P.J. Somerfield, A.M. Esteves, F.J.V. Castro, V.G.F. Genevois, and P.J.P. Santos. 2013. Nematode diversity in different microhabitats in a mangrove region. Marine Ecology 34: 257–268.CrossRefGoogle Scholar
  48. Platt, H.M., and R.M. Warwick. 1983. Freeliving marine nematodes. Part I. British Enoplids. Synopses of the British Fauna (new series) no. 28. Cambridge: Cambridge University Press.Google Scholar
  49. Platt, H.M., and R.M. Warwick. 1988. Freeliving marine nematodes. Part II. British Chromadorids. Synopses of the British Fauna (new series) no. 38. Leiden: E.J. Brill / W. Backhuys.Google Scholar
  50. Pusceddu, A., S. Bianchelli, J. Martín, P. Puig, A. Palanques, P. Masqué, and R. Danovaro. 2014. Chronic and intensive bottom trawling impairs deep-sea biodiversity and ecosystem functioning. Proceedings of the National Academy of Sciences 111: 8861–8866.CrossRefGoogle Scholar
  51. Qin, P., and C.X. Zhong. 1992. Applied studies on Spartina. China: Ocean Press.Google Scholar
  52. Riera, R., J. Nuñez, M. Brito, and F. Tuya. 2012. Differences in diversity, structure, and variability between intertidal and subtidal meiofaunal assemblages. Ciencias Marinas 38: 677–693.CrossRefGoogle Scholar
  53. Sahoo, G., S.R. Suchiang, and Z.A. Ansari. 2013. Meiofauna-mangrove interaction: a pilot study from a tropical mangrove habitat. Cahiers de Biologie Marine 54: 349–358.Google Scholar
  54. Saintilan, N., N.C. Wilson, K. Rogers, A. Rajkaran, and K.W. Krauss. 2014. Mangrove expansion and salt marsh decline at mangrove poleward limits. Global Change Biology 20: 147–157.CrossRefGoogle Scholar
  55. Sasekumar, A. 1994. Meiofauna of a mangrove shore on the west coast of peninsular Malaysia. Raffles Bulletin of Zoology 42: 901–915.Google Scholar
  56. Sawangarreruks, S., P. Yaowasooth, and S. Poovachiranon. 2011. Nematode diversity at Thachin River mouth, Samut Sakhon, Thailand. Publications of the Seto Marine Biological Laboratory 41: 25–34.CrossRefGoogle Scholar
  57. Semprucci, F., P. Colantoni, G. Baldelli, M. Rocchi, and M. Balsamo. 2010. The distribution of meiofauna on back-reef sandy platforms in the Maldives (Indian Ocean). Marine Ecology: An evolutionary perspective 31: 592–607.CrossRefGoogle Scholar
  58. Semprucci, F., M. Moreno, S. Sbrocca, M. Rocchi, G. Albertelli, and M. Balsamo. 2013a. The nematode assemblage as a tool for the assessment of marine ecological quality status: a case-study in the central Adriatic Sea. Mediterranean Marine Science 14: 48–57.CrossRefGoogle Scholar
  59. Semprucci, F., P. Colantoni, G. Baldelli, C. Sbrocca, M. Rocchi, and M. Balsamo. 2013b. Meiofauna associated with coral sediments in the Maldivian subtidal habitats (Indian Ocean). Marine Biodiversity 43: 189–198.CrossRefGoogle Scholar
  60. Semprucci, F., P. Colantoni, C. Sbrocca, G. Baldelli, and M. Balsamo. 2014. Spatial patterns of distribution of meiofaunal and nematode assemblages in the Huvadhoo lagoon (Maldives, Indian Ocean). Journal of Marine Biological Association of the United Kingdom 94: 1377–1385.CrossRefGoogle Scholar
  61. Semprucci, F., V. Losi, and M. Moreno. 2015. A review of Italian research on free-living marine nematodes and the future perspectives on their use as ecological indicators (EcoInds). Mediterranean Marine Science 16: 352–365.CrossRefGoogle Scholar
  62. Sheue, C.R., and H.Y. Liu. 2003. Kandelia obovata (Rhizophoraceae), a new mangrove species from eastern Asia. Taxon 52: 287–294.CrossRefGoogle Scholar
  63. Somerfield, P.J., and R.M. Warwick. 1996. Meiofauna in Marine Pollution Monitoring Programmes. a Laboratory Manual. Ministry of Agriculture, Fisheries and Food, Lowestoft.Google Scholar
  64. Steyaert, M., L. Moodley, T. Nadong, T. Moens, K. Soetaert, and M. Vincx. 2007. Responses of intertidal nematodes to short-term anoxic events. Journal of Experimental Marine Biology and Ecology 345: 175–184.CrossRefGoogle Scholar
  65. Teal, J.M., and W. Wieser. 1966. The distribution and ecology of nematodes in a Georgia salt marsh. Limnology and Oceanography 11: 217–222.CrossRefGoogle Scholar
  66. Tietjen, J.H. 1977. Population distribution and structure of the free-living nematodes of Long Island sound. Marine Biology 43: 123–136.CrossRefGoogle Scholar
  67. Vanaverbeke, J., T. Deprez, and M. Vincx. 2007. Changes in nematode communities at the long-term sand extraction site of the Kwintebank (southern bight of the North Sea). Marine Pollution Bulletin 54: 1351–1360.CrossRefGoogle Scholar
  68. Vanhove, S., M. Vincx, D.V. Gansbeke, W. Gijselinck, and D. Schram. 1992. The meiobenthos of five mangrove vegetation types in Gazi Bay, Kenya. Hydrobiologia 247: 99–108.CrossRefGoogle Scholar
  69. Wang, B.S., B.W. Liao, and Y.J. Wang. 2002. Mangrove forest ecosystem and its sustainable development in Shenzhen Bay. Beijing: Science Press.Google Scholar
  70. Wang, J.Q., X.D. Zhang, M. Nie, C.Z. Fu, J.K. Chen, and B. Li. 2008. Exotic Spartina alterniflora provides compatible habitats for native estuarine crab Sesarma dehaani in the Yangtze River estuary. Ecological Engineering 34: 57–64.CrossRefGoogle Scholar
  71. Wang, M., J.H. Zhang, Z.G. Tu, X.Q. Gao, and W.Q. Wang. 2011. Maintenance of estuarine water quality by mangroves occurs during flood periods: a case study of a subtropical mangrove wetland. Marine Pollution Bulletin 60: 2154–2160.CrossRefGoogle Scholar
  72. Warwick, R.M., H.M. Platt, and P.J. Somerfield. 1998. Freeliving Marine Nematodes. Part III. Monhysterids. Synopses of the British Fauna (new series) no. 53. Shrewsbury: Field Studies Council.Google Scholar
  73. Wei, S.D., Y.M. Lin, M.M. Liao, H.C. Zhou, and Y.Y. Li. 2012. Characterization and antioxidative properties of condensed tannins from the mangrove plant Aegiceras corniculatum. Journal of Applied Polymer Science 124: 2463–2472.CrossRefGoogle Scholar
  74. Wieser, W. 1953. Die Beziehung zwischen Mundhöhlengestalt, Ernährungsweise und Vorkommen bei freilebenden marinen Nematoden. Arkiv für Zoologie 4: 439–484.Google Scholar
  75. Wilkinson, C., and B. Salvat. 2012. Coastal resource degradation in the tropics: does the tragedy of the commons apply for coral reefs, mangrove forests and seagrass beds. Marine Pollution Bulletin 64: 1096–1105.CrossRefGoogle Scholar
  76. Xiang, P., Y.M. Lin, S. Ju, C. Xiang, and P. Lin. 2010. Tannin dynamics in hypocotyls and pericarps of Aegiceras corniculatum fruits during dry storage. African Journal of Agricultural Research 5: 1722–1732.Google Scholar
  77. Xuan, Q.N., A. Vanreusel, N.V. Thanh, and N. Smol. 2007. Biodiversity of meiofauna in the intertidal Khe Nhan mudflat, can Gio mangrove forest, Vietnam with special emphasis on free living nematodes. Ocean Science Journal 42: 135–152.CrossRefGoogle Scholar
  78. Yan, M.H., H.J. Xue, C.M. Lu, G.R. Wu, and P. Qin. 2006. The advantages and disadvantages of ecological engineering of Spartina in China. Journal of Biology 23: 5–8 [In Chinese with English abstract].Google Scholar
  79. Yodnarasri, S., S. Montani, K. Tada, S. Shibanuma, and T. Yamada. 2008. Is there any seasonal variation in marine nematodes within the sediments of the intertidal zone? Marine Pollution Bulletin 57: 149–154.CrossRefGoogle Scholar
  80. Zhang, Y.H., G.M. Huang, W.Q. Wang, L.Z. Chen, and G.H. Lin. 2012. Interactions between mangroves and exotic Spartina in an anthropogenically disturbed estuary in southern China. Ecology 93: 588–597.CrossRefGoogle Scholar
  81. Zhou, H. 2001. Effects of leaf litter addition on meiofaunal colonization of azoic sediments in a subtropical mangrove in Hong Kong. Journal of Experimental Marine Biology and Ecology 256: 99–121.CrossRefGoogle Scholar
  82. Zhou, H.C., N.F.Y. Tam, Y.M. Lin, S.D. Wei, and Y.Y. Li. 2012. Changes of condensed tannins during decomposition of leaves of Kandelia obovata in a subtropical mangrove swamp in China. Soil Biology & Biochemistry 44: 113–121.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  1. 1.Key Laboratory of the Ministry of Education for Coastal and Wetland EcosystemsXiamen UniversityXiamenChina
  2. 2.Third Institute of Oceanography, State Oceanic AdministrationXiamenChina
  3. 3.College of the Environment and EcologyXiamen UniversityXiamenChina

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