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Mangrove distribution in relation to seasonal water salinity and ion compartmentation: a field study along a freshwater-dominated river

  • Li Xu
  • Mao Wang
  • Changpeng Xin
  • Chao Liu
  • Wenqing WangEmail author
Primary Research Paper

Abstract

This study was designed to survey zonation and ion compartmentalization of mangroves in relation to water salinity along a freshwater-dominated river to reveal controlling factors of mangrove distribution, and to define differences in the mechanisms of adaptation to fluctuating salinity between true mangroves and mangrove associates. The water salinity along the river exhibited significant spatial and temporal variations, and true mangroves did not occur where freshwater was permanent. Both the true mangrove Aegiceras corniculatum and mangrove associate Hibiscus tiliaceus showed signs of preferential uptake of Cl and K+ at low-salinity sites, and Cl and Na+ exclusion at high-salinity sites. However, they differed in their selectivity for K+ over Na+: A. corniculatum preferentially absorbed K+ via root absorption, whereas H. tiliaceus preferentially controlled Na+ and promoted the transport of K+ from roots to stems. These findings indicate that, under fluctuating salinity, mangroves along the river maintained ion homeostasis in their tissues via preferential uptake of Cl and K+ under low salinity and exclusion of Cl and Na+ under high salinity. Water salinity regime and salt tolerance of mangrove species can explain the mangrove distribution along rivers.

Keywords

True mangrove Mangrove associate Salinity fluctuation Control factor Distribution 

Notes

Acknowledgements

We would like to thank Prof. Binyuan He and Prof. Guang-long Qiu, Guangxi Mangrove Research Center and many members of Beilunhekou National Nature Reserve for assistance with field work, to thank Prof. Nora F. Y. Tam, for her help of English writing and relevant comments on the manuscript. We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript. This study was jointly supported by the National Key Research and Development Program of China (No. 2016YFC0502904), the National Natural Science Foundation of China (No. 40776046).

Supplementary material

10750_2019_4119_MOESM1_ESM.docx (24 kb)
Supplementary material 1 (DOCX 23 kb)

References

  1. Ball, M. C., 1980. Patterns of secondary succession in a mangrove forest of Southern Florida. Oecologia 44: 226–235.PubMedCrossRefGoogle Scholar
  2. Ball, M. C., 1988. Ecophysiology of mangroves. Trees 2: 129–142.CrossRefGoogle Scholar
  3. Ball, M. C., 1996. Comparative ecophysiology of mangrove forest and tropical lowland moist forest. In Mulkey, S. S., R. L. Chazdon & A. P. Smith (eds.), Tropical Forest Plant Ecophysiology. Chapman and Hall, New York: 461–496.CrossRefGoogle Scholar
  4. Ball, M. C., 1998. Mangrove species richness in relation to salinity and waterlogging: a case study along the Adelaide River floodplain, northern Australia. Global Ecology and Biogeography Letters 7: 73–82.CrossRefGoogle Scholar
  5. Ball, M. C. & S. M. Pidsley, 1995. Growth responses to salinity in relation to distribution of two mangrove species, Sonneratia alba and S. lanceolata, in northern Australia. Functional Ecology 9: 77–85.CrossRefGoogle Scholar
  6. Barik, J., A. Mukhopadhyay, T. Ghosh, S. K. Mukhopadhyay, S. M. Chowdhury & S. Hazra, 2018. Mangrove species distribution and water salinity: an indicator species approach to Sundarban. Journal of Coastal Conservation 22: 361–368.CrossRefGoogle Scholar
  7. Bompy, F., G. Lequeue, D. Imbert & M. Dulormne, 2014. Increasing fluctuations of soil salinity affect seedling growth performances and physiology in three Neotropical mangrove species. Plant and Soil 380: 399–413.CrossRefGoogle Scholar
  8. Bunt, J. S., W. T. Williams & H. J. Clay, 1982. River water salinity and the distribution of mangrove species along several rivers in north Queensland. Australian Journal of Botany 30: 401–412.CrossRefGoogle Scholar
  9. Burchett, M. D., C. D. Field & A. Pulkownik, 1984. Salinity, growth and root respiration in the gray mangrove, Avicennia marina. Physiologia Plantarum 60: 113–118.CrossRefGoogle Scholar
  10. Chapman, V. J., 1976. Mangrove Vegetation. J. Cramer, Vaduz.Google Scholar
  11. Chen, D. M. & R. P. Yu, 1998. Salt-resistance and ionic characteristics of three wheat varieties under salt stress. Acta Pedologica Sinica. 35: 88–94.Google Scholar
  12. Connor, D. J., 1969. Growth of grey mangrove (Avicennia marina) in nutrient culture. Biotropica 1: 36–40.CrossRefGoogle Scholar
  13. Costa, P., A. Dórea, E. Mariano-Neto & F. Barros, 2015. Are there general spatial patterns of mangrove structure and composition along estuarine salinity gradients in Todos os Santos Bay? Estuarine, Coastal and Shelf Science 166: 83–91.CrossRefGoogle Scholar
  14. Critchley, C., 1982. Stimulation of photosynthetic electron transport in a salt-tolerant plant by high chloride concentrations. Nature 298: 483–485.CrossRefGoogle Scholar
  15. Dangremond, E. M., I. C. Feller & W. P. Sousa, 2015. Environmental tolerances of rare and common mangroves along light and salinity gradients. Oecologia 179: 1187–1198.PubMedCrossRefGoogle Scholar
  16. de Lacerda, L. D., C. E. Resende, D. V. Jose, J. C. Wasserman & M. C. Francisco, 1985. Mineral concentrations in leaves of mangrove trees. Biotropica 17: 260–262.CrossRefGoogle Scholar
  17. Duke, N. C., 1992. Mangrove floristics and biogeography. In Robertson, A. I. & D. M. Alongi (eds.), Tropical Mangrove Ecosystems (Coastal and Estuarine Studies 41). American Geophysical Union, Washington DC: 63–100.CrossRefGoogle Scholar
  18. Duke, N. C., M. C. Ball & J. C. Ellison, 1998. Factors influencing biodiversity and distributional gradients in mangroves. Global Ecology and Biogeography Letters 7: 27–47.CrossRefGoogle Scholar
  19. Ellison, A. M., B. B. Mukherjee & A. Karim, 2000. Testing patterns of zonation in mangroves: scale dependence and environmental correlates in the Sundarbans of Bangladesh. Journal of Ecology 88: 813–824.CrossRefGoogle Scholar
  20. Elster, C., 2000. Reasons for reforestation success and failure with three mangrove species in Colombia. Forest Ecology Management 131: 201–214.CrossRefGoogle Scholar
  21. Farnsworth, E., 2000. The ecology and physiology of viviparous and recalcitrant seeds. Annual Review of Ecology and Systematics 31: 107–138.CrossRefGoogle Scholar
  22. Flowers, T. J., M. A. Hajibagheri & N. J. W. Clipson, 1986. Halophytes. The Quarterly Review of Biology 61: 313–337.CrossRefGoogle Scholar
  23. He, B., Y. Cai, W. Ran & H. Jiang, 2014. Spatial and seasonal variations of soil salinity following vegetation restoration in coastal saline land in eastern China. Catena 118: 147–153.CrossRefGoogle Scholar
  24. Hogarth, P. J., 2015. The Biology of Mangroves and Seagrasses, 3rd ed. Oxford University Press, New York.CrossRefGoogle Scholar
  25. Hoppe-Speer, S. C. L., J. B. Adams, A. Rajkaran & D. Bailey, 2011. The response of the red mangrove Rhizophora mucronata Lam. to salinity and inundation in South Africa. Aquatic Botany 95: 71–76.CrossRefGoogle Scholar
  26. Jayatissa, L. P., F. Dahdouh-Guebas & N. Koedam, 2002. A review of the floral composition and distribution of mangroves in Sri Lanka. Botanical Journal of the Linnean Society 138: 29–43.CrossRefGoogle Scholar
  27. Joshi, G. V., 1973. Soil plant relationship in the plants of the saline soils of the Deccan. Proceedings of the Symposium on Deccan Trap Country (Poona, 1968). Indian National Science Academy 45: 30–38.Google Scholar
  28. Joshi, G. V. & B. B. Jamale, 1975. Ecological studies in mangroves of Terekhol and Vashisti rivers. Bulletin of the Department of Marine Sciences of the University of Cochin 7: 751–760.Google Scholar
  29. Kim, K., E. Seo, S. K. Chang, T. J. Park & S. J. Lee, 2016. Novel water filtration of saline water in the outermost layer of mangrove roots. Scientific Reports 6: 20426.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Krishnamurthy, P., P. A. Jyothi-Prakash, L. Qin, J. He, Q. Lin, C. S. Loh & P. P. Kumar, 2014. Role of root hydrophobic barriers in salt exclusion of a mangrove plant Avicennia officinalis. Plant, Cell and Environment 37: 1656–1671.PubMedCrossRefGoogle Scholar
  31. Lawton, J. R., A. Todd & D. K. Naidoo, 1981. Preliminary investigations into the structure of the roots of the mangroves, Avicennia marina and Bruguiera gymnorrhiza, in relation to ion uptake. New Phytologist 88: 713–722.CrossRefGoogle Scholar
  32. Li, N., S. Chen, X. Zhou, C. Li, J. Shao, R. Wang, E. Fritz, A. Hüttermann & A. Polle, 2008. Effect of NaCl on photosynthesis, salt accumulation and ion compartmentation in two mangrove species, Kandelia candel and Bruguiera gymnorhiza. Aquatic Botany 88: 303–310.CrossRefGoogle Scholar
  33. Lin, P., 1999. Mangrove Ecosystem in China. Science Press, Beijing.Google Scholar
  34. Lin, G. & L. S. L. da Sternberg, 1992. Comparative study of water uptake and photosynthetic gas exchange between scrub and fringe red mangroves, Rhizophora mangle L. Oecologia 90: 399–403.PubMedCrossRefGoogle Scholar
  35. Louda, S. M., 1989. Differential predation pressure: a general mechanism for structuring plant communities along complex environmental gradients? Trends in Ecology and Evolution 4: 158–159.CrossRefGoogle Scholar
  36. Lu, W., L. Chen, W. Wang, N. F. Y. Tam & G. Lin, 2013. Effects of sea level rise on mangrove Avicennia population growth, colonization and establishment: evidence from a field survey and greenhouse manipulation experiment. Acta Oecologica 49: 83–91.CrossRefGoogle Scholar
  37. Lugo, A. E. & S. C. Snedaker, 1974. The ecology of mangroves. Annual Review of Ecology and Systematics 5: 39–64.CrossRefGoogle Scholar
  38. Macnae, W., 1968. A general account of the fauna and flora of mangrove swamps and forests in the Indo-West-Pacific region. Advances in Marine Biology 6: 73–270.CrossRefGoogle Scholar
  39. Mallery, C. H. & H. J. Teas, 1984. The mineral ion relations of mangroves I. Root cell compartments in a salt excluder and a salt secreter species at low salinities. Plant & Cell Physiology 25: 1123–1131.Google Scholar
  40. Marschner, P., 2012. Mineral Nutrition of Higher Plants, 3rd ed. Academic Press, New York.Google Scholar
  41. Mitsch, W. J. & J. G. Gosselink, 2000. Wetlands, 3rd ed. Wiley, New York.Google Scholar
  42. Naidoo, G., O. Hiralal & Y. Naidoo, 2011. Hypersalinity effects on leaf ultrastructure and physiology in the mangrove Avicennia marina. Flora 206: 814–820.CrossRefGoogle Scholar
  43. Nguyen, H. T., D. E. Stanton, N. Schmitz, G. D. Farquhar & M. C. Ball, 2015. Growth responses of the mangrove Avicennia marina to salinity: development and function of shoot hydraulic systems require saline conditions. Annals of Botany 115: 397–407.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Omer, L. S., S. M. Horvath & F. Setaro, 1983. Salt regulation and leaf senescence in aging leaves of Jaumea carnosa (Less.) gray (Asteraceae), a salt marsh species exposed to NaCl stress. American Journal of Botany 70: 363–368.CrossRefGoogle Scholar
  45. Parida, A. K. & A. B. Das, 2005. Salt tolerance and salinity effect on plants: a review. Ecotoxicology and Environmental Safety 60: 324–349.PubMedCrossRefGoogle Scholar
  46. Parida, A. K., A. B. Das & B. Mittra, 2004. Effects of salt on growth, ion accumulation, photosynthesis and leaf anatomy of the mangrove, Bruguiera parviflora. Trees—Structure and Function 18: 167–174.CrossRefGoogle Scholar
  47. Pitman, M. G., 1984. Transport across the root and shoot/root interactions. In Staples, R. C. & G. H. Toennissen (eds), Salinity Tolerance in Plants: Strategies for Crop Improvement. Wiley, New York: 93–123.Google Scholar
  48. Roose, J. L., K. M. Wegener, & H. B. Pakrasi, 2007. The extrinsic proteins of Photosystem II. Photosynthesis Research 92: 369–387.PubMedCrossRefGoogle Scholar
  49. Scholander, P. F., 1968. How mangroves desalinate seawater. Physiologia Plantarum 21: 251–261.CrossRefGoogle Scholar
  50. Shabala, S. & T. A. Cuin, 2007. Potassium transport and plant salt tolerance. Physiologia Plantarum 133: 651–669.CrossRefGoogle Scholar
  51. Short, F. T., S. Kosten, P. A. Morgan, S. Malone & G. E. Moore, 2016. Impacts of climate change on submerged and emergent wetland plants. Aquatic Botany 135: 3–17.CrossRefGoogle Scholar
  52. Smith III, T. J., 1987. Effects of light and intertidal position on seedling survival and growth in tropical tidal forests. Journal of Experimental Marine Biology and Ecology 110: 133–146.CrossRefGoogle Scholar
  53. Smith III, T. J., 1992. Forest structure. In Robertson, A. I. & D. M. Alongi (eds), Tropical Mangrove Ecosystems (Coastal and Estuarine Series 41). American Geophysical Union, Washington DC: 101–136.CrossRefGoogle Scholar
  54. Smith III, T. J. & N. C. Duke, 1987. Physical determinants of inter-estuary variation in mangrove species richness around the tropical coastline of Australia. Journal of Biogeography 14: 9–19.CrossRefGoogle Scholar
  55. Tang, X. L., X. M. Mu, H. B. Shao, H. Y. Wang & M. Brestic, 2015. Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology. Critical Reviews in Biotechnology 35: 425–437.PubMedCrossRefGoogle Scholar
  56. Tomlinson, P. B., 2016. The Botany of Mangrove, 2nd ed. Cambridge University Press, New York.CrossRefGoogle Scholar
  57. Ukpong, I. E., 1994. Soil-vegetation interrelationships of mangrove swamps as revealed by multivariate analyses. Geoderma 64: 167–181.CrossRefGoogle Scholar
  58. Ungar, I. A., 1991. Ecophysiology of Vascular Halophytes. CRC Press, Florida.Google Scholar
  59. Waisel, Y., A. Eshel & M. Agami, 1986. Salt balance of leaves of the mangrove Avicennia marina. Physiologia Plantarum 67: 67–72.CrossRefGoogle Scholar
  60. Wang, W. & P. Lin, 1999. Transfer of salt and nutrients in Bruguiera gymnorrhiza leaves during development and senescence. Mangroves and Salt Marshes 3: 1–7.CrossRefGoogle Scholar
  61. Wang, W. & P. Lin, 2003. Element distribution in mangroves and salt-tolerant mechanism. Scientia Silvae Sinicae 39: 30–36.Google Scholar
  62. Wang, W., X. Li & M. Wang, 2019. Propagule dispersal determines mangrove zonation at intertidal and estuarine scales. Forests 10: 245.CrossRefGoogle Scholar
  63. Watson, J. G., 1928. Mangrove forest of the Malay Peninsula. Dissertation. Malayan Forest Records, No. 6. Forest Department, Kuala Lumpur.Google Scholar
  64. Zhu, Z., J. Chen & H. L. Zheng, 2012. Physiological and proteomic characterization of salt tolerance in a mangrove plant, Bruguiera gymnorrhiza (L.) Lam. Tree Physiology 32: 1378–1388.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Key Laboratory of the Coastal and Wetland Ecosystems (Xiamen University), Ministry of Education, College of the Environment & EcologyXiamen UniversityXiamenChina

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