Advertisement

Estuaries and Coasts

, Volume 41, Issue 3, pp 908–920 | Cite as

Geographical Distance and Large Rivers Shape Genetic Structure of Avicennia officinalis in the Highly Dynamic Sundarbans Mangrove Forest and Ganges Delta Region

  • Ludwig TriestEmail author
  • Sharmin Hasan
  • Perboti Rani Mitro
  • Dennis J. R. De Ryck
  • Tom Van der Stocken
Article

Abstract

The Ganges Delta and Sundarbans comprise the largest continuous mangrove area in the world. These mangroves are subjected to high riverine and tidal dynamics, and the coastline irregularity is characterized by many north-to-south oriented rivers that may hamper dispersal of mangrove propagules. Whereas connectivity levels and resulting population genetic structure often can be explained by ocean currents, other factors may control estuarine-scale mangrove genetic patterns and limit gene flow even between sites in close geographic proximity. We investigated whether the complex estuarine coastline in the Ganges Delta and Sundarbans shaped the genetic structure of Avicennia officinalis populations across regions and rivers at various distances (ca. 1 to 265 km). Using nine microsatellite loci, 433 individuals from 14 populations revealed predominant outcrossing and a high level of genetic variation when compared to other Avicennia species. A moderate but significant level of differentiation was detected among populations (F ST = 0.09), and a principal coordinate analysis clearly separated populations of the Chittagong coastline from the Sundarbans. An individual-based Bayesian analysis also indicated those two gene pools. Genetic distances across the whole region could best be explained by cumulative river width and geographical distance separating the populations. Within the Sundarban region, the low genetic differentiation of A. officinalis populations indicated a continuous distribution model with a smooth isolation-by-distance that gradually increased across large rivers shaping the genetic structure of A. officinalis in the Ganges Delta. These findings indicated that in addition to geographical distance, rivers might act as physical barriers, affect gene flow and shape genetic connectivity. This and detailed population genetic information should be incorporated into the ongoing afforestation or restoration strategies in and outside of the Sundarbans mangrove forest.

Keywords

Mangrove Avicennia Microsatellites Genetic structure Dispersal Conservation 

Notes

Acknowledgements

Sharmin Hasan and Perboti Mitro received a VLIR-ICP scholarship for ‘Biology: Human Ecology’. We are also grateful to Jahangir Alom for assistance in the field and to Tim Sierens for lab assistance.

Funding Information

We thank the Vrije Universiteit Brussel for research funding (BAS42).

References

  1. Abdul, A.M. 2014. Analysis of Environmental Pollution in Sundarbans. American Journal of Biomedical and Life Sciences 2: 98–107.CrossRefGoogle Scholar
  2. Allendorf, F.W., and G. Luikart. 2007. Conservation and the Genetics of Populations. Carlton: Blackwell publishing.Google Scholar
  3. Aluri, R.J.S. 1990. Observations on the floral biology of certain mangroves. Proceedings of the National Science Academy, India Section B: Biological Science 56: 367–374.Google Scholar
  4. Arnaud-Haond, S., S. Teixeira, S. Massa, C. Billot, P. Seanger, G. Coupland, C.M. Duarte, and E.A. Serrão. 2006. Genetic structure and mating system at range-edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Molecular Ecology 15: 3515–3525.CrossRefGoogle Scholar
  5. Balke, T., T.J. Bouma, E.M. Horstman, E.L. Webb, P.L.A. Erftemeijer, and M.J. Herman. 2011. Windows of opportunity: thresholds to mangrove seedling establishment on tidal flats. Marine Ecology Progress Series 440: 1–9.CrossRefGoogle Scholar
  6. Brammer, H. 2014. Bangladesh’s dynamic coastal regions and sea-level rise. Climate Risk Management 1: 51–62.CrossRefGoogle Scholar
  7. Cerón-Souza, I., E. Bermingham, W.O. McMillan, and F.A. Jones. 2012. Comparative genetic structure of two mangrove species in Caribbean and Pacific estuaries of Panama. BMC Evolutionary Biology 12: 205.CrossRefGoogle Scholar
  8. Cerón-Souza, I., N. Toro-Perea, and H. Cardenas-Henao. 2005. Population Genetic Structure of Neotropical Mangrove Species on the Colombian Pacific Coast: Avicennia germinans (Avicenniaceae). Biotropica 37: 258–265.CrossRefGoogle Scholar
  9. Chowdhury, M.A.M. 1996. Notes on natural regeneration potential of major mangrove species in degrading Sundarbans ecosystem of Bangladesh. In Proceedings of Ecotone IV: ecology and management of mangrove restoration and regeneration in east and southeast Asia, ed. C. Khemnark, 104–118. Suart Thani: Thailand.Google Scholar
  10. Clarke, P.J. 1993. Dispersal of gray mangrove (Avicennia marina) propagules in southeastern Australia. Aquatic Botany 45: 195–204.CrossRefGoogle Scholar
  11. Crawford, N.G. 2010. SMOGD: software for the measurement of genetic diversity. Molecular Ecology Research 10: 556–557.CrossRefGoogle Scholar
  12. De Ryck, D.J.R., N. Koedam, T. Van der Stocken, R.M. van der Ven, J. Adams, and L. Triest. 2016. Dispersal limitation of the mangrove Avicennia marina at its South African range limit in strong contrast to connectivity in its core East African region. Marine Ecology Progress Series 545: 123–134.CrossRefGoogle Scholar
  13. de Wilde, K. 2011. Moving coastlines: emergence and use of land in the Ganges-Brahmaputra-Meghna estuary. Dhaka: University Press Limited.Google Scholar
  14. Duke, N., E. Lo, and M. Sun. 2002. Global distribution and genetic discontinuities of mangroves—emerging patterns in the evolution of Rhizophora. Trees—Structure and Function 16: 65–79.CrossRefGoogle Scholar
  15. Duke, N., J.A.H. Benzie, J.A. Goodall, and E.R. Ballment. 1998. Genetic structure and evolution of species in the mangrove genus Avicennia (Avicenniaceae) in the Indo-West Pacific. Evolution 52: 1612–1626.CrossRefGoogle Scholar
  16. Evanno, G., S. Regnaut, and J. Goudet. 2005. Detecting the number of clusters of individuals using software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.CrossRefGoogle Scholar
  17. Geng, Q., C. Lian, S. Goto, J. Tao, and T. Hogetsus. 2007. Isolation and characterization of 10 new compound microsatellite markers for a mangrove tree species, Avicennia marina (Forsk.) Vierh. (Avicenniaceae). Molecular Ecology Notes 7: 1208–1210.CrossRefGoogle Scholar
  18. Geng, Q., C. Lian, S. Goto, J. Tao, M. Kimura, M.D.S. Islam, and T. Hogetsus. 2008. Mating system, pollen and propagule dispersal, and spatial genetic structure in a high-density population of the mangrove tree Kandelia candel. Molecular Ecology 17: 4724–4739.CrossRefGoogle Scholar
  19. Giang, L.H., P.N. Hong, M.S. Tuan, and K. Harada. 2003. Genetic variation of Avicennia marina (Forsk.) Vierh. (Avicenniaceae) in Vietnam revealed by microsatellite and AFLP markers. Genes and Genetic Systems 78: 399–407.CrossRefGoogle Scholar
  20. Gilg, M.R., and T.J. Hilbish. 2003. The geography of marine larval dispersal: coupling genetics with fine-scale physical oceanography. Ecology 84: 2989–2998.CrossRefGoogle Scholar
  21. Gopal, B., and M. Chauhan. 2006. Biodiversity and its conservation in the Sundarban Mangrove Ecosystem. Aquatic Science 68: 338–354.CrossRefGoogle Scholar
  22. Goudet, J. 2001. FSTAT version 2.9.3.: a program to estimate and test gene diversities and fixation indices (update from version 1.2 Goudet 1995): a computer program to calculate F-statistic. Journal of Heredity 86: 485–486 http://www.unil.ch/izea/softwares/fstat.html.CrossRefGoogle Scholar
  23. Hardy, O.J., and X. Vekemans. 2002. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618–620.CrossRefGoogle Scholar
  24. Hermansen, T.D., D.G. Roberts, M. Toben, T.E. Minchinton, and D.J. Ayre. 2015. Small urban stands of the mangrove Avicennia marina are genetically diverse but experience elevated inbreeding. Estuaries and Coasts 38: 1898–1907.CrossRefGoogle Scholar
  25. Homer, L. 2009. Population structure and distance of gene flow in Avicennia marina (Forsk.) Vierh. (Avicenniaceae) on a local/ regional scale in the Northern Rivers of New South Wales, Australia. PhD Thesis, Southern Cross University, Australia.Google Scholar
  26. Hussain, S.A., and R. Badola. 2010. Valuing mangrove benefits: contribution of mangrove forests to local livelihoods in Bhitarkanika Conservation Area, East Coast of India. Wetlands Ecology and Management 18: 321–331.CrossRefGoogle Scholar
  27. Islam, S.M., and A.M. Wahab. 2005. A review on the present status and management of mangrove wetland habitat resources in Bangladesh with emphasis on mangrove fisheries and aquaculture. Hydrobiologia 542: 165–190.CrossRefGoogle Scholar
  28. Islam, S.N., and A. Gnauck. 2011. Water salinity investigation in the Sundarbans rivers in Bangladesh. International Journal on Water 6: 74–91.CrossRefGoogle Scholar
  29. Jakobsen, F.L., M.H. Azam, and M. Mahboob-Ul-Kabir. 2002. Residual flow in the Meghna Estuary on the coastline of Bangladesh. Estuarine, Coastal and Shelf Science 55: 587–597.CrossRefGoogle Scholar
  30. Jost, L. 2008. G ST and its relatives do not measure differentiation. Molecular Ecology 17: 4015–4026.CrossRefGoogle Scholar
  31. Kairo, J.G., F. Dahdouh-Guebas, J. Bosire, and N. Koedam. 2001. Restoration and management of mangrove systems—a lesson for and from the East African region. South African Journal of Botany 67: 383–389.CrossRefGoogle Scholar
  32. Kennedy, J.P., P.W. Maria, C.E. Proffitt, W.A. Boeger, A.M. Stanford, and D.J. Devlin. 2016. Postglacial expansion pathways of red mangrove, Rhizophora mangle, in the Caribbean Basin and Florida. American Journal of Botany 103 (2): 260–276.CrossRefGoogle Scholar
  33. Kool, J.D., C.B. Paris, S. Andréfouët, and R.K. Cowen. 2010. Complex migration and the development of genetic structure in subdivided populations: an example from Caribbean coral reef ecosystems. Ecography 33: 597–606.Google Scholar
  34. Lee, S.Y., J.H. Primavera, F. Dahdouh-Guebas, K. McKee, J.O. Bosire, S. Cannicci, K. Diele, F. Fromard, N. Koedam, C. Marchand, I. Mendelssohn, N. Mukherjee, and S. Record. 2014. Ecological role and services of tropical mangrove ecosystems: a reassessment. Global Ecology and Biogeography 23: 726–743.CrossRefGoogle Scholar
  35. Maguire, T.L., K.J. Edwards, P. Saenger, and R. Henry. 2000a. Characterisation and analysis of microsatellite loci in a mangrove species, Avicennia marina (Forsk.) Vierh. (Avicenniaceae). Theoretical and Applied Genetics 101: 279–285.CrossRefGoogle Scholar
  36. Maguire, T.L., P. Saenger, P. Baverstock, and R. Henry. 2000b. Microsatellite analysis of genetic structure in the mangrove species Avicennia marina (Forsk.) Vierh. (Avicenniaceae). Molecular Ecology 9: 1853–1862.CrossRefGoogle Scholar
  37. Maguire, T.L., R. Peakall, and P. Saenger. 2002. Comparative analysis of genetic diversity in the mangrove species Avicennia marina (Forsk.) Vierh. (Avicenniaceae) detected by AFLPs and SSRs. Theoretical and Applied Genetics 104: 338–398.CrossRefGoogle Scholar
  38. Matthijs, S., J. Tack, D. Van Speybroeck, and N. Koedam. 1999. Mangrove species zonation and soil redox state, sulphide concentration and salinity in Gazi Bay (Kenya), a preliminary study. Mangroves Salt Marshes 3: 243–249.CrossRefGoogle Scholar
  39. McGuinness, K.A. 1997. Dispersal, establishment and survival of Ceriops tagal propagules in a north Australian mangrove forest. Oecologia 109: 80–87.Google Scholar
  40. Melville, F., and M. Burchett. 2002. Genetic variation in Avicennia marina in three estuaries of Sydney (Australia) and implications for rehabilitation and management. Marine Pollution Bulletin 44: 469–479.CrossRefGoogle Scholar
  41. Mori, G.M., M.I. Zucchi, and A.P. Souza. 2015. Multiple-geographic-scale genetic structure of two mangrove tree species: the roles of mating system, hybridization, limited dispersal and extrinsic factors. PloS One 10 (2): e0118710.CrossRefGoogle Scholar
  42. Nathan, R., and H.C. Muller-Landau. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology and Evolution 15: 278–285.CrossRefGoogle Scholar
  43. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.Google Scholar
  44. Nettel, A., and R.S. Dodd. 2007. Drifiting propagules and receding swamps: genetic footprints of mangrove recolonization and dispersal along tropical coasts. Evolution 61: 958–971.Google Scholar
  45. Ngeve, N.M., T. Van der Stocken, D. Menemenlis, N. Koedam, and L. Triest. 2016. Contrasting effects of historical sea level rise and contemporary ocean currents on regional gene flow of Rhizophora racemosa in Eastern Atlantic mangroves. PloS One 11 (3): e0150950.CrossRefGoogle Scholar
  46. Peakall, R., and P.E. Smouse. 2006. GENALEX 6: genetic analysis in Excel, Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295.CrossRefGoogle Scholar
  47. Peterson, J.M., and S.S. Bell. 2012. Tidal events and salt-marsh structure influence black mangrove (Avicennia germinans) recruitment across an ecotone. Ecology 93: 1648–1658.CrossRefGoogle Scholar
  48. Piry, S., G. Luikart, and J.M. Cornuet. 1999. Bottleneck: A computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90: 502–503.CrossRefGoogle Scholar
  49. Pritchard, J.K., M. Stephens, and P. Donnelly. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.Google Scholar
  50. Rahman, M.M., M.M. Rahman, and K.S. Islam. 2010. The causes of deterioration of Sundarban mangrove forest ecosystem of Bangladesh: conservation and sustainable management issues. Aquaculture, Aquarium, Conservation and Legislation 3: 77–90.Google Scholar
  51. Raju, A.J.S., P.V.S. Rao, R. Kumar, and R.S. Mohan. 2012. Pollination biology of the crypto-viviparous Avicennia species (Avicenniaceae). Journal of Threatened Taxa 4: 3377–3389.CrossRefGoogle Scholar
  52. Rao, R.V., and T. Hodgkin. 2001. Genetic diversity and conservation and utilization of plant genetic resources. Plant Cell Tissue Organ Culture 68: 1–19.Google Scholar
  53. Rathcke, B.J., and C.L. Landry. 2003. Dispersal and recruitment of white mangrove on San Salvador Island, Bahamas after Hurricane Floyd. In Proceedings of the ninth symposium on the natural history of the Bahamas, ed. David L. Smith and Sherilyn Smith, 34–40. Bahamas: Gerace Research Center, San Salvador.Google Scholar
  54. Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219–1228.Google Scholar
  55. Salas-Leiva, D.E., V.M. Mayor-Duran, and N. Toro-Perea. 2009. Genetic diversity of black mangrove (Avicennia germinans) in natural and reforested areas of Salamanca Island Parkway, Colombian Caribbean. Hydrobiologia 620: 17–24.CrossRefGoogle Scholar
  56. Sarwar, M.G.M., and C.D. Woodroffe. 2013. Rates of shoreline change along the coast of Bangladesh. Journal of Coastal Conservation 17: 515–526.CrossRefGoogle Scholar
  57. Seidensticker, J., and A.M. Hai. 1983. The Sundarbans wildlife management plan, conservation in the Bangladesh coastal zone, 120. Gland: IUCN.Google Scholar
  58. Selkoe, K.A., J.R. Watson, C. White, T.B. Horin, M. Iacchei, S. Mitarai, D.A. Siegel, S.D. Gaines, and R.J. Toonen. 2010. Taking the chaos out of genetic patchiness: seascape genetics reveals ecological and oceanographic drivers of genetic patterns in three temperate reef species. Molecular Ecology 19: 3708–3726.CrossRefGoogle Scholar
  59. Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236: 787–792.CrossRefGoogle Scholar
  60. Sousa, W.P., P.G. Kennedy, B.J. Mitchell, and B.M. Ordónez. 2007. Supply-side ecology in mangroves: do propagule dispersal and seedling establishment explain forest structure? Ecological Monographs 77: 53–76.CrossRefGoogle Scholar
  61. Smith, T.J. 1987. Seed predation in relation to tree dominance and distribution in mangrove forests. Ecology of Freshwater Fish 68: 266–273.Google Scholar
  62. Takayama, K., M. Tamura, Y. Tateishi, E.L. Webb, and T. Kajita. 2013. Strong genetic structure over the American continents and transoceanic dispersal in the mangrove genus Rhizophora (Rhizophoraceae) revealed by broad-scale nuclear and chloroplast DNA analysis. American Journal of Botany 100: 1191–1201.CrossRefGoogle Scholar
  63. Teixeira, S., A. Arnaud-Haond, M. Duarte, and O.E. Serra. 2003. Polymorphic microsatellite DNA markers in the mangrove tree Avicennia alba. Molecular Ecology Notes 3: 544–546.CrossRefGoogle Scholar
  64. Tomlinson, P.B. 1986. The botany of mangroves. London: Cambridge University Press.Google Scholar
  65. Triest, L. 2008. Molecular ecology and biogeography of mangrove trees towards conceptual insights on gene flow and barriers: a review. Aquatic Botany 89: 138–154.CrossRefGoogle Scholar
  66. Van der Stocken, T., D.J.R. De Ryck, T. Balke, T.J. Bouma, F. Dahdouh-Guebas, and N. Koedam. 2013. The role of wind in hydrochorous mangrove propagule dispersal. Biogeosciences 10: 3635–3647.CrossRefGoogle Scholar
  67. Van der Stocken, T., B. Vanschoenwinkel, D.J.R. De Ryck, T.J. Bouma, F. Dahdouh-Guebas, and N. Koedam. 2015. Interaction between water and wind as a driver of passive dispersal in mangroves. PloS One 10 (3): e0121593.CrossRefGoogle Scholar
  68. Van der Stocken, T., J. López-Portillo, and N. Koedam. 2017. Seasonal release of propagules in mangroves—Assessment of current data. Aquatic Botany (in press).  https://doi.org/10.1016/j.aquabot.2017.02.001.
  69. Van Nedervelde, F., S. Cannicci, N. Koedam, J. Bosire, and F. Dahdouh-Guebas. 2015. What regulates crab predation on mangrove propagules? Acta Oecologica 63: 63–70.CrossRefGoogle Scholar
  70. Van Oosterhout, C., W.F. Hutchinson, D.P. Wills, and P. Shipley. 2004. Micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.CrossRefGoogle Scholar
  71. Walters, B.B., P. Rönnbäck, J. Kovacs, B. Crona, S. Hussain, R. Badola, J. Primavera, E.B. Barbier, and F. Dahdouh-Guebas. 2008. Ethnobiology, socio-economics and adaptive management of mangroves: a review. Aquatic Botany 89: 220–236.CrossRefGoogle Scholar
  72. Waters, J.M. 2008. Marine biogeographical disjunction in temperate Australia: historical landbridge, contemporary currents, or both? Diversity and Distributions 14: 692–700.CrossRefGoogle Scholar
  73. Wee, A.K.S., K. Takayama, T. Asakawa, B. Thompson, S. Ornizal, N.X. Sungkaew, M. Tung, K.K. Nazre, H.T.W. Soe, Y. Tan, S. Watano, T. Kajita Baba, and E.L. Webb. 2014. Oceanic currents, not land masses, maintain the genetic structure of the mangrove Rhizophora mucronata Lam. (Rhizophoraceae) in Southeast Asia. Journal of Biogeography 41: 954–964.CrossRefGoogle Scholar
  74. Weir, B.S., and C.C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.Google Scholar
  75. Wells, S., C. Ravilious, and E. Corcoran. 2006. In the front line: shoreline protection and other ecosystem services from mangroves and coral reefs. Cambridge: UNEP/Earthprint.Google Scholar
  76. White, C., K.A. Selkoe, J. Watson, D.A. Siegel, D.C. Zacherl, and R.J. Toonen. 2010. Ocean currents help explain population genetic structure. Proceedings of the Royal Society of London B 277: 1685–1694. Le 1.Google Scholar
  77. Wright, S. 1943. Isolation by distance. Genetics 28: 114–138.Google Scholar
  78. Ye, Y., N.F.Y. Tam, Y.S. Wong, and C.Y. Lu. 2003. Growth and physiological responses of two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to waterlogging. Environmental and Experimental Botany 49: 209–221.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  • Ludwig Triest
    • 1
    Email author
  • Sharmin Hasan
    • 1
    • 2
  • Perboti Rani Mitro
    • 1
    • 3
  • Dennis J. R. De Ryck
    • 1
  • Tom Van der Stocken
    • 1
  1. 1.Ecology and Biodiversity, Plant Biology and Nature ManagementVrije Universiteit BrusselBrusselsBelgium
  2. 2.Department of BotanyJagannath UniversityDhakaBangladesh
  3. 3.Bangladesh Agricultural UniversityMymensinghBangladesh

Personalised recommendations