Sexual reproduction vs. clonal propagation in the recovery of a seagrass meadow after an extreme weather event
DOI:
https://doi.org/10.3989/scimar.04843.06AKeywords:
seagrass recovery, Zostera marina, genotypic diversity, impact, disturbance, life traitsAbstract
Marine flowering plants can reproduce sexually and clonally, and the relative contribution of these two modes can be dependent on the environmental conditions. Zostera marina, a seagrass widely distributed in the northern hemisphere, can form annual and perennial meadows with different proportions of sexual versus clonal propagation depending on the environmental disturbance regime. We study the hypothesis that the contribution of sexual propagation varies during the recovery of a seagrass meadow. In this case study, we compare the proportion of sexual versus clonal propagation of a perennial Z. marina meadow before its disappearance due to winter storms and after recovery. Before disturbance, genotypic diversity was high, indicating frequent sexual reproduction events likely to create an abundant seed bank. Seedling germination allowed the population to recover after the extreme disturbance. As months passed, seedlings became rare and finally absent, giving place to adult shoots. In an advanced stage of colonization, the shoots colonized the area by vegetative growth, which lowered the genotypic diversity. Despite this reduction over time, the genotypic diversity of the new meadow is still high, demonstrating the importance of sexual reproduction in meadow recovery and persistence.
Downloads
References
Alberto F. 2009. MsatAllele_1.0: an R package to visualize the binning of microsatellite alleles. J. Hered. 100: 394-397. https://doi.org/10.1093/jhered/esn110 PMid:19126639
Alexandre A., Santos R., Serrão E. 2005. Effects of clam harvesting on sexual reproduction of the seagrass Zostera noltii. Mar. Ecol. Prog. Ser. 298: 115-122. https://doi.org/10.3354/meps298115
Arnaud-Haond S., Belkhir K. 2007. GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol. Ecol. Resour. 7: 15-17. https://doi.org/10.1111/j.1471-8286.2006.01522.x
Bell S.S., Fonseca M.S., Kenworthy W.J. 2008. Dynamics of a subtropical seagrass landscape: links between disturbance and mobile seed banks. J. Landsc. Ecol. 23: 67-74. https://doi.org/10.1007/s10980-007-9137-z
Bos A.R., Bouma T.J., de Kort G.L., et al. 2007. Ecosystem engineering by annual intertidal seagrass beds: sediment accretion and modification. Estuar. Coast. Shelf Sci. 74: 344-348. https://doi.org/10.1016/j.ecss.2007.04.006
Cabaço S., Santos R. 2012. Seagrass reproductive effort as an ecological indicator of disturbance. Ecol. Indic. 23: 116-122. https://doi.org/10.1016/j.ecolind.2012.03.022
Craine J.M. 2009. Resource strategies of wild plants. Princeton University Press. https://doi.org/10.1515/9781400830640
Cunha A.H., Assis J.F., Serrão E.A. 2013. Seagrasses in Portugal: a most endangered marine habitat. Aquat. Bot. 104: 193-203. https://doi.org/10.1016/j.aquabot.2011.08.007
Cunha A.H., Erzini K., Serrão E.A., et al. 2014. Biomares, a LIFE project to restore and manage the biodiversity of Prof. Luiz Saldanha Marine Park. J. Coast. Conserv. 18: 643-655. https://doi.org/10.1007/s11852-014-0336-x
Den Hartog C. 1970. The sea-grasses of the world. North-Holland Pub. Co., Amsterdam.
Den Hartog C. 1987. "Wasting disease" and other dynamic phenomena in Zostera beds. Aquat. Bot. 27: 3-14 https://doi.org/10.1016/0304-3770(87)90082-9
Diekmann O.E., Serrao E.A. 2012. Range-edge genetic diversity: locally poor extant southern patches maintain a regionally diverse hotspot in the seagrass Zostera marina. Mol. Ecol. 21: 1647-1657. https://doi.org/10.1111/j.1365-294X.2012.05500.x PMid:22369278
Dorken M.E., Eckert C.G. 2001. Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J. Ecol. 89: 339-350. https://doi.org/10.1046/j.1365-2745.2001.00558.x
Doyle J.J., Doyle J.L. 1988. Natural interspecific hybridization in eastern North American Claytonia. Am. J. Bot. 75: 1238-1246. https://doi.org/10.1002/j.1537-2197.1988.tb08838.x
Evans S.M., Vergés A., Poore A.G. 2017. Genotypic diversity and short-term response to shading stress in a threatened seagrass: Does low diversity mean low resilience? Front. Plant. Sci. 8: 1417. https://doi.org/10.3389/fpls.2017.01417 PMid:28855915 PMCid:PMC5557787
Excoffier L., Smouse P.E., Quattro J.M. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491.
Goudet J. 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. J. Hered. 86: 485-486. https://doi.org/10.1093/oxfordjournals.jhered.a111627
Greve T.M., Krause-Jensen D., Rasmussen M.B., et al. 2005. Means of rapid eelgrass (Zostera marina L.) recolonisation in former dieback areas. Aquat. Bot. 82: 143-156. https://doi.org/10.1016/j.aquabot.2005.03.004
Hammerstrom K.K., Kenworthy W.J., Fonseca M.S., et al. 2006. Seed bank, biomass, and productivity of Halophila decipiens, a deep water seagrass on the west Florida continental shelf. Aquat. Bot. 84: 110-120. https://doi.org/10.1016/j.aquabot.2005.08.002
Hemminga M.A., Duarte C.M. 2000. Seagrass ecology. Cambridge University Press. https://doi.org/10.1017/CBO9780511525551
Hughes A.R., Stachowicz, J.J. 2004. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc. Natl. Acad. Sci. 101: 8998-9002. https://doi.org/10.1073/pnas.0402642101 PMid:15184681 PMCid:PMC428461
Jarvis J.C., Moore K.A. 2010. The role of seedlings and seed bank viability in the recovery of Chesapeake Bay, USA, Zostera marina populations following a large-scale decline. Hydrobiologia 649: 55-68. https://doi.org/10.1007/s10750-010-0258-z
Jarvis J.C., Moore K.A., Kenworthy W.J. 2014. Persistence of Zostera marina L. (eelgrass) seeds in the sediment seed bank. J. Exp. Mar. Biol. Ecol. 459: 126-136. https://doi.org/10.1016/j.jembe.2014.05.024
Keddy C.J., Patriquin D.G. 1978. An annual form of eelgrass in Nova Scotia. Aquat. Bot. 5: 163-170. https://doi.org/10.1016/0304-3770(78)90059-1
Kim T.H., Rark S.R., Kim Y.K., et al. 2008. Growth dynamics and carbon incorporation of the seagrass Zostera marina L. in Jindong Bay and Gamak Bay on the Southern Coast of Korea. Algae 23: 241-250. https://doi.org/10.4490/ALGAE.2008.23.3.241
Kim S.H., Kim J.H., Park S.R., et al. 2014. Annual and perennial life history strategies of Zostera marina populations under different light regimes. Mar. Ecol. Prog. Ser. 509: 1-13. https://doi.org/10.3354/meps10899
Larkum A.W.D., Den Hartog C. 1989. Evolution and biogeography of seagrasses. Biology of seagrasses. In: Larkum A.W., McComb A.J., et al. (eds), Biology of seagrasses: a treatise on the biology of seagrasses with special reference to the Australian region. Elsevier, Amsterdam, pp. 112-156.
Marbà N., Duarte C.M. 1998. Rhizome elongation and seagrass clonal growth. Mar. Ecol. Prog. Ser. 174: 269-280. https://doi.org/10.3354/meps174269
Marion S.R., Orth R.J. 2010. Innovative techniques for large-scale seagrass restoration using Zostera marina (eelgrass) seeds. Restor. Ecol. 18: 514-526. https://doi.org/10.1111/j.1526-100X.2010.00692.x
Massa S.I., Paulino C.M., Serrão E.A., et al. 2013. Entangled effects of allelic and clonal (genotypic) richness in the resistance and resilience of experimental populations of the seagrass Zostera noltii to diatom invasion. BMC Ecol. 13: 39. https://doi.org/10.1186/1472-6785-13-39 PMid:24152760 PMCid:PMC3818440
Meirmans P.G., Van Tienderen P.H. 2004. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 4: 792-794. https://doi.org/10.1111/j.1471-8286.2004.00770.x
Meling-López A.E., Ibarra-Obando S.E. 1999. Annual life cycles of two Zostera marina L. populations in the Gulf of California: contrasts in seasonality and reproductive effort. Aquat. Bot. 65: 59-69. https://doi.org/10.1016/S0304-3770(99)00031-5
Michalakis Y., Excoffier L. 1996. A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142: 1061-1064.
Olesen B. 1999. Reproduction in Danish eelgrass (Zostera marina L.) stands: size-dependence and biomass partitioning. Aquat. Bot. 65: 209-219. https://doi.org/10.1016/S0304-3770(99)00041-8
Olesen B., Sand-Jensen K. 1994. Patch dynamics of eelgrass Zostera marina. Mar. Ecol. Prog. Ser. 106: 147-156. https://doi.org/10.3354/meps106147
Orth R.J., Luckenbach M.L., Marion S.R., et al. 2006. Seagrass recovery in the Delmarva coastal bays, USA. Aquat. Bot. 84: 26-36. https://doi.org/10.1016/j.aquabot.2005.07.007
Paetkau D., Calvert W., Stirling I., et al. 1995. Microsatellite analysis of population structure in Canadian polar bears. Mol. Ecol. 4: 347-354. https://doi.org/10.1111/j.1365-294X.1995.tb00227.x PMid:7663752
Park S.R., Kim Y.K., Kim J.H., et al. 2011. Rapid recovery of the intertidal seagrass Zostera japonica following intense Manila clam (Ruditapes philippinarum) harvesting activity in Korea. J. Exp. Mar. Biol. Ecol. 407: 275-283. https://doi.org/10.1016/j.jembe.2011.06.023
Paulo D., Cunha A.H., Boavida J., et al. 2019. Open coast seagrass restoration. Can we do it? Large scale seagrass transplants. Front. Mar. Sci. 6: 52. https://doi.org/10.3389/fmars.2019.00052
Qin L.Z., Li W.T., Zhang X.M., et al. 2014. Sexual reproduction and seed dispersal pattern of annual and perennial Zostera marina in a heterogeneous habitat. Wetl. Ecol. Manag. 22: 671-682. https://doi.org/10.1007/s11273-014-9363-5
Qin L.Z., Li W.T., Zhang X., et al. 2016. Recovery of the eelgrass Zostera marina following intense Manila clam Ruditapes philippinarum harvesting disturbance in China: The role and fate of seedlings. Aquat. Bot. 130: 27-36. https://doi.org/10.1016/j.aquabot.2016.01.002
R Core Development Team. 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/
Rafajlovi? M., Kleinhans D., Gulliksson C., et al. 2017. Neutral processes forming large clones during colonization of new areas. J. Evol. Biol. 30: 1544-1560. https://doi.org/10.1111/jeb.13124 PMid:28557006
Reusch T.B.H. 2000. Five microsatellite loci in eelgrass Zostera marina and a test of cross-species amplification in Z. noltii and Z. japonica. Mol. Ecol. 9: 371-373. https://doi.org/10.1046/j.1365-294x.2000.00874-4.x PMid:10736037
Reusch T.B.H. 2001. Fitness-consequences of geitonogamous selfing in a clonal marine angiosperm (Zostera marina). J. Evol. Biol. 14: 129-138. https://doi.org/10.1046/j.1420-9101.2001.00257.x PMid:29280577
Reusch T.B. 2006. Does disturbance enhance genotypic diversity in clonal organisms? A field test in the marine angiosperm Zostera marina. Mol. Ecol. 15: 277-286. https://doi.org/10.1111/j.1365-294X.2005.02779.x PMid:16367846
Reusch T.B.H., Stam W.T., Olsen J.L. 2000. A microsatellite-based estimation of clonal diversity and population subdivision in Zostera marina, a marine flowering plant. Mol. Ecol. 9: 127-140. https://doi.org/10.1046/j.1365-294x.2000.00839.x PMid:10672157
Reusch T.B., Ehlers A., Hämmerli A., et al. 2005. Ecosystem recovery after climatic extremes enhanced by genotypic diversity. Proc. Natl. Acad. Sci. USA 102: 2826-2831. https://doi.org/10.1073/pnas.0500008102 PMid:15710890 PMCid:PMC549506
Santamaría-Gallegos N.A., Sánchez-Lizaso J.L., Félix-Pico E.F. 2000. Phenology and growth cycle of annual subtidal eelgrass in a subtropical locality. Aquat. Bot. 66: 329-339. https://doi.org/10.1016/S0304-3770(99)00082-0
Short F.T., Carruthers T.J.R., Waycott M., et al. 2010. Zostera marina. The IUCN red list of threatened species. Version 2014.2.
Stam T.B.R., Wytze T., Olsen J.L. 1999. Microsatellite loci in eelgrass Zostera marina reveal marked polymorphism within and among populations. Mol. Ecol. 8: 317-321. https://doi.org/10.1046/j.1365-294X.1999.00531.x PMid:10065546
Tanner C.E., Parham T. 2010. Growing Zostera marina (eelgrass) from seeds in land-based culture systems for use in restoration projects. Rest. Ecol. 18: 527-537. https://doi.org/10.1111/j.1526-100X.2010.00693.x
van Lent F., Verschuure J.M. 1994. Intraspecific variability of Zostera marina L. (eelgrass) in the estuaries and lagoons of the southwestern Netherlands. I. Population dynamics. Aquat. Bot. 48: 31-58. https://doi.org/10.1016/0304-3770(94)90072-8
Waycott M., Duarte C.M., Carruthers T.J., et al. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. USA 106: 12377-12381. https://doi.org/10.1073/pnas.0905620106 PMid:19587236 PMCid:PMC2707273
Williams S.L. 1988. Disturbance and recovery of a deep-water Caribbean seagrass bed. Mar. Ecol. Prog. Ser. 42: 63-71. https://doi.org/10.3354/meps042063
Published
How to Cite
Issue
Section
License
Copyright (c) 2011 Consejo Superior de Investigaciones Científicas (CSIC)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the printed and online versions of this Journal are the property of Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.All contents of this electronic edition, except where otherwise noted, are distributed under a “Creative Commons Attribution 4.0 International” (CC BY 4.0) License. You may read here the basic information and the legal text of the license. The indication of the CC BY 4.0 License must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the published by the Editor, is not allowed.