Hidden founders? Strong bottlenecks and fine-scale genetic structure in mangrove populations of the Cameroon Estuary complex

Hydrobiologia

Volumn 803, Issue 1, 2017, Pages 189-207

  Ngeve, Magdalene N ^a   Van der Stocken, Tom ^a   Menemenlis, Dimitris ^b   Koedam, Nico ^a   Triest, Ludwig ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

African mangroves; Connectivity; Dispersal; Effective population size; Gene flow; Hydrochory; Mangrove expansion; Ocean currents

Indexed keywords

CONNECTIVITY; DISPERSAL; EFFECTIVE POPULATION SIZE; GENE FLOW; GENETIC MARKER; GENETIC STRUCTURE; HYDROCHORY; MANGROVE; OCEANIC CURRENT; PROPAGULE; RANGE EXPANSION; RECOLONIZATION; SEA SURFACE;

CAMEROON;

RHIZOPHORA; RHIZOPHORA RACEMOSA; RHIZOPHORACEAE;

EID: 85028978099     PISSN: 00188158     EISSN: 15735117     Source Type: Journal    
DOI: 10.1007/s10750-017-3369-y     Document Type: Article

References (78)

1. Addisalem, A. B., J. Duminil, D. Wouters, D. F. Bongers & M. J. M. Smulders, 2016. Fine-scale spatial genetic structure in the frankincense tree Boswellia papyrifera (Del.) Hochst. and implications for conservation. Tree Genetics & Genomes 12: 86.
2. Alemagi, D., P. M. Oben & J. Ertel, 2006. Mitigating industrial pollution along the atlantic coast of cameroon: an overview of government efforts. Environmentalist 26: 41–50.
3. Allen, J. A. & K. W. Krauss, 2006. Influence of propagule flotation longevity and light availability on establishment of introduced mangrove species in Hawaii. Pacific Science 60: 367–376.
4. Arnaud-Haond, S., S. Teixeira, S. I. Massa, C. Billot, P. Saenger, G. Coupland, C. M. Duarte & E. A. Serrão, 2006. Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Molecular Ecology 15: 3515–3525.
5. Balloux, F. & N. Lugon-Moulin, 2002. The estimation of population differentiation with microsatellite markers. Molecular Ecology 11: 155–165.
6. Beerli, P., 2006. Comparison of Bayesian and maximum likelihood inference of population genetic parameters. Bioinformatics 22: 341–345.
7. Beerli, P. & M. Palczewski, 2010. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185: 313–326.
8. Cerón-Souza, I., E. Bermingham, W. O. McMillan & F. A. Jones, 2012. Comparative genetic structure of two mangrove species in Caribbean and Pacific estuaries of Panama. BMC Evolutionary Biology 12: 205.
9. Chen, L., L. Xu & H. Huanga, 2007. Genetic diversity and population structure in Vallisneria spinulosa (Hydrocharitaceae). Aquatic Botany 86: 46–52.
10. Chung, M. Y. & M. G. Chung, 2013. Significant spatial aggregation and fine-scale genetic structure in the homosporous fern Cyrtomium falcatum (Dryopteridaceae). New Phytologist 199: 663–672.
11. Corcoran, E., C. Ravilious, & M. Skuja, 2007. Mangroves of Western and Central Africa. By ISBN: 978-92-807-2792-0. UNEP-WCMC Biodiversity Series 26 (2007).
12. De Ryck, D. J. R., E. M. R. Robert, N. Schmitz, T. Van der Stocken, D. Di Nitto, F. Dahdouh-Guebas & N. Koedam, 2012. Size does matter, but not only size: two alternative dispersal strategies for viviparous mangrove propagules. Aquatic Botany 103: 66–73.
13. De Ryck, D. J. R., N. Koedam, T. Van der Stocken, R. M. van der Ven, J. Adams & 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.
14. Din, N., R. J. Priso, M. Kenne, D. E. Ngollo & F. Blasco, 2002. Early growth stages and natural regeneration of Avicennia germinans (L.) stearn in the Wouri estuarine mangroves (Douala-Cameroon). Wetlands Ecology and Management 10: 461–472.
15. Din, N., P. Saenger, R. J. Priso, D. S. Dibong & F. Blasco, 2008. Logging activities in mangrove forests: a case study of Douala Cameroon. African Journal of Environmental Science and Technology 2: 22–30.
16. Drexler, J. Z., 2001. Maximum longevities of Rhizophora apiculata and R. mucronata propagules. Pacific Science 55: 17–22.
17. Ellison, J. C., & I. Zouh, 2012. Vulnerability to climate change of mangroves: Assessment from Cameroon, Central Africa. Biology 1: 617–638. doi:10.3390/biology1030617.
18. Epperson, B. K., 2007. Plant dispersal, neighbourhood size and isolation by distance. Molecular Ecology 16: 3854–3865.
19. Epperson, B. K. & L. Tianquan, 1996. Measurement of genetic structure within populations using Moran’s spatial autocorrelation statistics. Proceedings of the National Academy of Science USA 93: 10528–10532.
20. FAO, 2011. FAO/Global environment facility project document. CBSP—sustainable community-based management and conservation of mangrove ecosystems in Cameroon. GEF project ID: 3821, FAO project symbol: GCP/CMR/030/GFF.
21. Feka, N. Z. & A. G. Ajonina, 2011. Drivers causing decline of mangrove in West-Central Africa: a review. International Journal of Biodiversity Science, Ecosystem Services & Management 7: 217–230.
22. Feka, Z. N. & I. Morrison, 2017. Managing mangroves for coastal ecosystems change: a decade and beyond of conservation experiences and lessons for and from west-central Africa. Journal of Ecology and The Natural Environment 9: 99–123.
23. Geng, Q., C. Lian, S. Goto, J. Tao, M. Kimura, M. S. Islam & T. Hogetsu, 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.
24. Gillis, L. G., M. Zimmer & T. J. Bouma, 2016. Mangrove leaf transportation: do mimic Avicennia and Rhizophora roots retain or donate leaves? Marine Ecology Progress Series 551: 107–115.
25. Hamilton, S. E. & D. Casey, 2016. Creation of a high spatio-temporal resolution global database of continuous mangrove forest cover for the 21st century. Global Ecology and Biogeography 25: 729–738.
26. Hamrick, J. L. & J. D. Nason, 1996. Consequence of dispersal in plants. In Rhodes, O. E., K. C. Ronald & M. H. Smith (eds), Population Dynamics in Ecological Space and Time. The University of Chicago Press, Chicago: 203–235.
27. Hardy, O. J. & X. Vekemans, 2002. SPAGeDi: a versatile compute program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618–620.
28. Hardy, O. J., N. Charbonnel, H. Fréville & M. Heuertz, 2003. Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163: 1467–1482.
29. Hardy, O. J., S. Gonzalphalez-Martnunez, B. Colas, H. Friotaville, A. Mignot & I. Olivieri, 2004. Fine-scale genetic structure and gene dispersal in Centaurea corymbosa (Asteraceae). II. Correlated paternity within and among sibships. Genetics 168: 1601–1614.
30. Helsen, K., H. Jacquemyn & O. Honnay, 2015. Hidden founder effects: small-scale spatial genetic structure in recently established populations of the grassland specialist plant Anthyllis vulneraria. Molecular Ecology 24: 2715–2728.
31. Hill, C., D. Menemenlis, B. Ciotti & C. Henze, 2007. Investigating solution convergence in a global ocean model using a 2048-processor cluster of distributed shared memory machines. Scientific Programming 12: 107–115.
32. Honnay, O., H. Jacquemy, K. Nackaerts, P. Breyne & K. Van Looy, 2010. Patterns of population genetic diversity in riparian and aquatic plant species along rivers. Journal of Biogeography 37: 1730–1739.
33. Islam, M. S., C. Lian, N. Kameyama & T. Hogetsu, 2014. Low genetic diversity and limited gene flow in a dominant mangrove tree species (Rhizophora stylosa) at its northern biogeographical limit across the chain of three Sakishima islands of the Japanese archipelago as revealed by chloroplast and nuclear SSR analysis. Plant Systematics and Evolution 300: 1123–1136.
34. Jalonen, R., L. T. Hong, S. L. Lee, J. Loo & L. Snook, 2014. Integrating genetic factors into management of tropical Asian production forests: a review of current knowledge. Forest Ecology and Management 315: 191–201.
35. Kennedy, J. P., M. W. Pil, C. E. Proffitt, W. A. Boeger, A. M. Stanford & D. J. Devlin, 2016. Postglacial expansion pathways of red mangrove, Rhizophora mangle, in the Caribbean Basin and Florida. American Journal of Botany 103: 260–276.
36. Kinlan, B. P. & S. D. Gaines, 2003. Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84: 2007–2020.
37. Kudoh, H. & D. F. Whigham, 1997. Microgeographic genetic structure and gene flow in Hibiscus moscheutos (Malvaceae) populations. American Journal of Botany. 84: 1285–1293.
38. Latch, E. K., D. M. Reding, J. R. Heffelfinger, C. H. Alcalá-Galván & O. E. Rhodes, 2014. Range-wide analysis of genetic structure in a widespread, highly mobile species (Odocoileus hemionus) reveals the importance of historical biogeography. Molecular Ecology 23: 3171–3190. PMID: 24863151.
39. Leonardi, S., P. Piovani, M. Scalfi, A. Piotti, R. Giannini & P. Menozzi, 2012. Effect of habitat fragmentation on the genetic diversity and structure of peripheral populations of beech in Central Italy. Journal of Heredity 103: 408–417.
40. Li, J., Y. Yang, Q. Chen, L. Fang, Z. He, W. Guo, S. Qiao, Z. Wang, M. Guo, C. Zhong, R. Zhou & S. Shi, 2016. Pronounced genetic differentiation and recent secondary contact in the mangrove tree Lumnitzera racemosa revealed by population genomic analyses. Scientific Reports 6: 29486.
41. Loveless, M. D. & J. L. Hamrick, 1984. Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15: 65–95.
42. Maguire, T. L., P. Saenger, P. Baverstock & R. Henry, 2000. Microsatellite analysis of genetic structure in the mangrove species Avicennia marina (Forsk.) Vierh. (Avicenniaceae). Molecular Ecology 9: 1853–1862.
43. Menemenlis, D., J. M. Campin, P. Heimbach, C. Hill, T. Lee, A. Nguyen, M. Schodlok & H. Zhang, 2008. ECCO2: high resolution global ocean and sea ice data synthesis. Mercator Ocean Quarterly Newsletter 31: 13–21.
44. Millán-Aguilar, O., M. Manzano-Sarabia, A. Nettel-Hernanz, R. S. Dodd, M. Á. Hurtado-Oliva & E. Velázquez-Velázquez, 2016. Genetic Diversity of the Black Mangrove Avicennia germinans (L.) Stearn in Northwestern Mexico. Forests 7: 197.
45. Mori, G. M., M. I. Zucchi & 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.
46. Nathan, R., F. M. Schurr, O. Spiegel, O. Steinitz, A. Trakhtenbrot & A. Tsoar, 2008. Mechanisms of long-distance seed dispersal. Trends in Ecology & Evolution 23: 638–647.
47. Ndjebet., C. & P. Ngokoy, 2014. Master plan for Cameroon Estuary mangrove forests. ITTO Tropical Forest Update 23:13–15. http://www.itto.int/partner/id=4110.
48. Nfotabong-Atheull, A., N. Din, S. N. Longonje, N. Koedam & F. Dahdouh-Guebas, 2009. Commercial activities and subsistence utilization of mangrove forests around the Wouri estuary and the Douala-Edea reserve (Cameroon). Journal of Ethnobiology and Ethnomedicine. doi:10.1186/1746-4269-5-35.
49. Nfotabong-Atheull, A., N. Din, L. G. E. Koum, B. Satyanarayana, N. Koedam & F. Dahdouh-Guebas, 2011. Assessing forest products usage and local residents’ perception of environmental changes in peri-urban and rural mangroves of Cameroon, Central Africa. Journal of Ethnobiology and Ethnomedicine. doi:10.1186/1746-4269-7-41.
50. Nfotabong-Atheull, A., N. Din & F. Dahdouh-Guebas, 2013. Qualitative and quantitative characterization of mangrove vegetation structure and dynamics in a peri-urban settings of Douala (Cameroon): an approach using airborn imagery. Estuaries and Coasts 36: 1181–1192.
51. Ngeve, M. N., M. Leermakers, M. Elskens & M. Kochzius, 2015. Assessment of trace metal pollution in sediments and intertidal fauna at the coast of Cameroon. Environmental Monitoring and Assessment 187: 337.
52. Ngeve, M. N., T. Van der Stocken, D. Menemenlis, N. Koedam & L. Triest, 2016a. 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.
53. Ngeve, M. N., T. Van der Stocken, T. Sierens, N. Koedam & L. Triest, 2016b. Bidirectional gene flow on a mangrove river landscape and between-catchment dispersal of Rhizophora racemosa (Rhizophoraceae). Hydrobiologia. doi:10.1007/s10750-016-3021-2.
54. Nilsson, C., R. L. Brown, R. Jansson & D. M. Merritt, 2010. The role of hydrochory in structuring riparian and wetland vegetation. Biological reviews of the Cambridge Philosophical Society 85: 837–858.
55. Pandey, M. & O. P. Rajora, 2012. Higher fine-scale genetic structure in peripheral than in core populations of a long-lived and mixed-mating conifer—eastern white cedar (Thuja occidentalis L.). BMC Evolutionary Biology 12: 48.
56. Peakall, R. & P. E. Smouse, 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28: 2537–2539.
57. Peakall, R., M. Ruibal & D. B. Lindenmayer, 2003. Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57: 1182–1195.
58. Pil, M. W., M. R. T. Boeger, V. C. Muschner, M. R. Pie, A. Ostrensky & W. A. Boeger, 2011. Postglacial north–south expansion of populations of Rhizophora mangle (Rhizophoraceae) along the Brazilian coast revealed by microsatellite analysis. American Journal of Botany 98: 1031–1039.
59. Piry, S., G. Luikart, & J.-M. Cornuet, 1999. BOTTLENECK: A program for detecting recent effective population size reductions from allele data frequencies. http://www1.montpellier.inra.fr/CBGP/software/Bottleneck/bottleneck.html.
60. Rabinowitz, D., 1978. Dispersal properties of mangrove propagules. Biotropica 10: 47–57.
61. Rocha, C. B., T. K. Chereskin, S. T. Gille & D. Menemenlis, 2016. Mesoscale to submesoscale wavenumber spectra in Drake Passage. Journal of Physical Oceanography 46: 601–620.
62. Saenger, P., & M. F. Bellan, 1995. The mangrove vegetation of the Atlantic Coast of Africa: a review. Universite’ de Toulouse, Toulouse, France. Copyright P. Saenger 1995.
63. Smith, W. H. F., & D. T. Sandwell, 1977. Global seafloor topography from satellite altimetry and ship depth soundings. Science 277: 1957–1962.
64. Smouse, P. E. & R. Peakall, 1999. Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82: 561–573.
65. Sousa, W. P., P. G. Kennedy, B. J. Mitchell & L. Ordóñez, 2007. Supply-side ecology in mangroves: do propagule dispersal and seedling establishment explain forest structure? Ecological Monographs 77: 53–76.
66. Steele, O., 2006. Natural and anthropogenic biogeography of mangroves in the Southwest Pacific. PhD Dissertation. University of Hawaii, Manoa.
67. Tonné, N., N. Koedam, N. Buls, J. De Mey, H. Beeckman & E. M. R. Robert, 2016. Computed tomography and light microscopy: combining visualisation techniques in the study of mangrove seedling development. The International Association of Wood Anatomists 37: 28–47.
68. Tonné, N., H. Beeckman, E. M. R. Robert & N. Koedam, 2017. Towards an unknown fate: the floating behaviour of recently abscised propagules from wide ranging Rhizophoraceae mangrove species. Aquatic Botany. doi:10.1016/j.aquabot.2017.01.008.
69. Trakhtenbrot, A., R. Nathan, G. Perry & D. M. Richardson, 2005. The importance of long-distance dispersal in biodiversity conservation. Diversity and Distributions 11: 173–181.
70. Van Campo, E. & M. D. Bengo, 2004. Mangrove palynology in recent marine sediments off Cameroon. Marine Geology 208: 315–330.
71. Van der Stocken, T., D. J. R. De Ryck, T. Balke, T. J. Bouma, F. Dahdouh-Guebas & N. Koedam, 2013. The role of wind in hydrochorous mangrove propagule dispersal. Biogeosciences 10: 3635–3647.
72. Van der Stocken, T., B. Vanschoenwinkel, D. J. R. De Ryck, T. J. Bouma, F. Dahdouh-Guebas & N. Koedam, 2015a. Interaction between water and wind as a driver of passive dispersal in mangroves. PLoS One 10(3): e0121593.
73. Van der Stocken, T., D. J. R. De Ryck, B. Vanschoenwinkel, E. Deboelpaep, T. J. Bouma, F. Dahdouh-Guebas & N. Koedam, 2015b. Impact of landscape structure on propagule dispersal in mangrove forests. Marine Ecology Progress Series 524: 95–106.
74. Vekemans, X. & O. J. Hardy, 2004. New insights from fine-scale spatial genetic structure analyses in plant populations. Molecular Ecology 13: 921–935.
75. Vergara, M., M. P. Basto, M. J. Madeira, B. J. Gómez-Moliner, M. Santos-Reis, C. Fernandes & A. Ruiz-González, 2015. Inferring population genetic structure in widely and continuously distributed carnivores: the stone marten (Martes foina) as a case study. PLoS ONE 10: e0134257.
76. Vigouroux, Y., J. S. Jaqueth, Y. Matsuoka, O. S. Smith, W. D. Beavis, J. S. C. Smith & J. Doebley, 2002. Rate and pattern of mutation at microsatellite loci in maize. Molecular Biology and Evolution 19: 1251–1260.
77. Wee, A. K. S., K. Takayama, T. Asakawa, B. Thompson, S. Sungkaew, N. X. Tung, M. Nazre, K. K. Soe, H. T. W. Tan, Y. Watano, S. Baba, T. Kajita & 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.
78. Wells, G. P. & A. G. Young, 2002. Effect of seed dispersal on genetic structure in populations of Rutidosis leptorrhychoides with different levels of correlated paternity. Genetics Research 79: 219–226.