Skip to main content

Advertisement

SpringerLink
Log in

Small Urban Stands of the Mangrove Avicennia marina are Genetically Diverse but Experience Elevated Inbreeding

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Anthropogenic impacts contribute to the fragmentation of urban mangrove forests, and in the Sydney region of Australia, Avicennia marina is commonly found in small stands of <50 adult trees that have altered pollinator services. However, genetic diversity may not vary with stand size because insufficient time has passed since stands were established or pollen and propagule dispersal are sufficient to overwhelm the effects of genetic drift and founder events. We tested the predictions that, despite the potential of mangroves for dispersal of propagules by water and long distance dispersal of pollen by honeybees, fragmentation and localized foraging by honeybees causes small stands of A. marina to display reduced genetic diversity and elevated inbreeding. Using four microsatellite markers, we quantified the genetic and genotypic diversity present within samples of 20 adults taken from three large (>1500 trees), intermediate (300–500 trees) and small (<50 trees) stands within each of two urbanized estuaries and estimated mating system parameters using progeny arrays for sets of five adults within the large and small stands. We detected no significant effect of stand size on levels of single-locus genetic diversity. There were low, although significant, levels of allelic differentiation within (F SE = 0.021, P = 0.003) and among (F ET = 0.055, P = 0.005) estuaries but no evidence of isolation by distance. In contrast, our analysis of progeny arrays revealed that, while all stands displayed high levels of biparental inbreeding, an expected consequence of pollination by honeybees, current outcrossing rates (t m ) were significantly lower in small (0.55) as compared to large (0.75) stands. The genetic makeup of the adult populations imply that stands are interconnected and suggest little impact of habitat fragmentation, while the progeny arrays suggest that plants within small stands may display reduced fitness.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguilar, R., L. Ashworth, L. Galetto, and M.A. Aizen. 2006. Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecology Letters 9: 968–980.

    Article  Google Scholar 

  • Aizen, M.A., L. Ashworth, and G. Leonardo. 2002. Reproductive success in fragmented habitats: do compatibility systems and pollination specialization matter? Journal of Vegetation Science 13: 885–892.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Barrett, S.C.H., and J.R. Kohn. 1991. Genetic and evolutionary consequences of small population size in plants. In Genetics and conservation in rear plants, ed. D.A. Falk and K.E. Holsinger, 3–30. New York: Oxford University Press.

    Google Scholar 

  • Clarke, P.J. 1993. Dispersal of gray mangrove (Avicennia marina) propagules in southeastern Australia. Aquatic Botany 45: 195–204.

    Article  Google Scholar 

  • Clarke, P.J., and P.J. Myerscough. 1991. Floral biology and reproductive phenology of Avicennia marina in South-eastern Australia. Australian Journal of Botany 39: 283–293.

    Article  Google Scholar 

  • Collinge, S.K. 2009. Ecology of fragmented landscapes. Baltimore: Johns Hopkins University Press.

    Google Scholar 

  • Doyle, J., and J.L. Doyle. 1987. Genomic plant DNA preparation from fresh tissue—CTAB method. Phytochemical Bulletin 19: 11.

    Google Scholar 

  • Duke, N.C. 2006. Australia’s mangroves. The authoritative guide to Australia’s mangrove plants. Brisbane: University of Queensland.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Dunstan, D.J. 1990. Some early environmental problems and guidelines in New South Wales estuaries. Wetlands (Australia) 9: 1–6.

    Google Scholar 

  • England, P.R., F. Beynon, D.J. Ayre, and R.J. Whelan. 2001. A molecular genetic assessment of mating-system variation in a naturally bird-pollinated shrub: contributions from birds and introduced honeybees. Conservation Biology 15: 1645–1655.

    Article  Google Scholar 

  • Ghazoul, J. 2005. Pollen and seed dispersal among dispersed plants. Biological Reviews 80: 413–443.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Goudet, J. 2001. FSTAT version 2.9.3, a program to estimate and test gene diversities and fixation indices. http://www2.unil.ch/popgen/softwares/fstat.htm.

  • Hamrick, J.L., and A. Schnabel. 1985. Understanding the genetic structure of plant populations: some old problems and a new approach. In Population genetics in forestry. Lecture notes in biomathematics 60, ed. H.R. Gregorious, 50–70. Berlin: Springer.

    Chapter  Google Scholar 

  • Hermansen, T.D., D.R. Britton, T.E. Minchinton, and D.J. Ayre. 2014a. Identifying the real pollinators? Exotic honeybees are the dominant flower visitors and only effective pollinators of Avicennia marina in Australian temperate mangroves. Estuaries and Coasts 37: 621–635.

    Article  Google Scholar 

  • Hermansen, T.D., D.J. Ayre, and T.E. Minchinton. 2014b. Effects of stand size on pollination in temperate populations of the mangrove Avicennia marina. Plant Ecology 215: 1153–1162.

    Article  Google Scholar 

  • 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.

  • Jensen, J.L., A.J. Jeffrey, and S.T. Kelley. 2005. Isolation by distance, web service. BMC Genetics 6: 13.

    Article  Google Scholar 

  • Kahrood, H.V., S.A.A. Korori, M. Pirseyedi, A. Shirvany, and A. Danehkar. 2008. Genetic variation of mangrove species Avicennia marina in Iran revealed by microsatellite markers. African Journal of Biotechnology 7: 3017–3021.

    CAS  Google Scholar 

  • Llorens, T.M., D.J. Ayre, and R.J. Whelan. 2004. Evidence for ancient genetic subdivision among recently fragmented populations of the endangered shrub Grevillea caleyi (Proteaceae). Heredety 92: 519–526.

    Article  CAS  Google Scholar 

  • Lomov, B., D.A. Keith, and D.F. Hochuli. 2010. Pollination and plant reproductive success in restored urban landscapes dominated by a pervasive exotic pollinator. Landscape and Urban Planning 96: 232–239.

    Article  Google Scholar 

  • Maguire, T.L., P. Saenger, P. Baverstock, and R. Henry. 2000a. Microsatellite analysis of genetic structure in the mangrove species Avicennia marina (Forsk.) Vierh. (Avicenniaceae). Molecular Ecology 9: 1853–1862.

    Article  CAS  Google Scholar 

  • Maguire, T.L., K.J. Edwards, P. Saenger, and R. Henry. 2000b. Characterisation and analysis of microsatellite loci in a mangrove species, Avicennia marina, (forsk.) Vierh. (Avicenniaceae). Theoretical and Applied Genetics 101: 279–285.

    Article  CAS  Google Scholar 

  • McLoughlin, L.C. 2000. Estuarine wetlands distribution along the Parramatta River, Sydney, 1788–1940: implications for planning and conservation. Cunninghamia 6: 579–610.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Melville, F., M. Burchett, and A. Pulkownik. 2004. Genetic variation among age-classes of the mangrove Avicennia marina in clean and contaminated sediments. Marine Pollution Bulletin 49: 695–703.

    Article  CAS  Google Scholar 

  • Miller, M.P. 1997. Tools for population genetic analysis (TFPGA) version 1.3. http://www.marksgeneticsoftware.net/tfpga.htm.

  • Minchinton, T.E. 2006. Consequences of pre-dispersal damage by insects for the dispersal and recruitment of mangroves. Oecologia 148: 70–80.

    Article  Google Scholar 

  • Pahl, M., H. Zhu, J. Tautz, and S. Chang. 2011. Large scale homing in honeybees. PLOS One e19669. doi:10.1371/journal.pone.0019669.

  • Pasquet, R.S., A. Peltier, M.B. Hufford, E. Oudin, J. Saulnier, L. Paul, J.T. Knudsen, H.R. Herren, and P. Gepts. 2008. Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. PNAS 105: 13456–13461.

    Article  CAS  Google Scholar 

  • Paton, D.C. 1993. Honey-bees in the Australian environment. Does Apis mellifera disrupt or benefit the native biota? BioScience 43: 95–103.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Reed, D.H., and R. Frankham. 2003. Correlation between fitness and genetic diversity. Conservation Biology 17: 230–237.

    Article  Google Scholar 

  • Ritland, K. 2002. Extensions of models for the estimation of mating systems using n independent loci. Heredity 88: 221–228.

    Article  Google Scholar 

  • Ritland, K., and S.K. Jain. 1981. A model for the estimation of outcrossing rate and gene frequencies using n independent loci. Heredity 47: 35–52.

    Article  Google Scholar 

  • Roberts, D.G., K.M. Ottewell, R.J. Whelan, and D.J. Ayre. 2014. Is the post-disturbance composition of a plant population determined by selection for outcrossed seedlings or by the composition of the seedbank? Heredity 112: 409–414.

    Article  CAS  Google Scholar 

  • Rossetto, M., R. Jones, and J. Hunter. 2004. Genetic effects of rainforest fragmentation in an early successional tree (Elaeocarpus grandis). Heredity 93: 610–618.

    Article  CAS  Google Scholar 

  • Slatkin, M. 1993. Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47: 264–279.

    Article  Google Scholar 

  • Southwick, E.E., and S.L. Buchmann. 1995. Effects of horizon landmarks on homing success in honey bees. American Naturalist 146: 748–764.

    Article  Google Scholar 

  • Thorogood, C.A. 1985. Changes in the distribution of mangroves in the Port Jackson–Parramatta River estuary from 1930 to 1985. Wetlands (Australia) 5: 91–96.

    Google Scholar 

  • van Oosterhout, C., W.F. Hutchinson, P.M.D. Wills, and P. Shipley. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.

    Article  Google Scholar 

  • Weir, B.S., and C.C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.

    Article  Google Scholar 

  • West, R.J., C.A. Thorgorod, T.R. Walford, and R.J. Williams. 1985. An estuarine inventory for New South Wales Australia. NSW: Fisheries Bulletin 2, Department of Agriculture.

    Google Scholar 

  • Whelan, R.J., D.J. Ayre, and F.M. Beynon. 2009. The birds and the bees: pollinator behavior and variation in the mating system of the rare shrub Grevillea macleayana. Annals of Botany 103: 1395–1401.

    Article  Google Scholar 

  • Williams, D.A., Y. Wang, M. Borchetta, and M.S. Gaines. 2007. Genetic diversity and spatial structure of a keystone species in fragmented pine rockland habitat. Biological Conservation 138: 256–268.

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by a University of Wollongong postgraduate scholarship to TDH, by an ARC Discovery Grant to DJA and TEM and by the University of Wollongong’s Institute for Conservation Biology and Environmental Management.

Author information

Authors and Affiliations

  1. Institute for Conservation Biology and Environmental Management, School of Biological Sciences, University of Wollongong, Wollongong, NSW, 2522, Australia

    Tyge D. Hermansen, David G. Roberts, Marijana Toben, Todd E. Minchinton & David J. Ayre

Authors
  1. Tyge D. Hermansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David G. Roberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marijana Toben
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Todd E. Minchinton
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. David J. Ayre
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tyge D. Hermansen.

Additional information

Communicated by John C. Callaway

Appendix

Appendix

Table 2 Significance of linkage disequilibrium between pairs of microsatellite locus within individual stand
Full size table
Table 3 Hierarchical F statistics estimated over four microsatellite loci of adult A. marina plants in two urban estuaries where F ET is genetic variation between estuaries, F SE is genetic variation among stands within estuaries and F IS is the inbreeding coefficient
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hermansen, T.D., Roberts, D.G., Toben, M. et al. Small Urban Stands of the Mangrove Avicennia marina are Genetically Diverse but Experience Elevated Inbreeding. Estuaries and Coasts 38, 1898–1907 (2015). https://doi.org/10.1007/s12237-015-9955-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-015-9955-1

Keywords

Search

Navigation