Skip to main content
SpringerLink
Log in

Genetic structure and gene flow of eelgrass Zostera marina populations in Tokyo Bay, Japan: implications for their restoration

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Massive losses of eelgrass Zostera marina beds in Japan have occurred over the past 100 years. Toward their restoration, transplantation of eelgrass has been attempted in some areas, including Tokyo Bay. This study examined population genetic structures and gene flow in eelgrass in Tokyo Bay to establish guidelines for conducting restoration. Genotypes of a total of 360 individuals from 12 beds were determined using five microsatellite markers. The eelgrass beds in inner bay had above-average genetic diversity. A neighbor-joining tree based on F ST values among beds revealed that a strong gene flow had occurred among six beds in the inner bay. Genetic assignment testing of drifting shoots indicated that those with seeds migrate in both directions between the inner and outer bay. We suggested that the restoration of eelgrass in the innermost part of Tokyo Bay, where natural habitats have been lost, should be conducted using the inner bay beds.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aioi K, Nakaoka M, Kouchi N, Omori Y (2000) A new record of Zostera asiatica Miki (Zosteraceae) in Funakoshi Bay, Iwate Prefecture. Otsuchi Mar Sci 25:23–26

    Google Scholar 

  • Alberto F, Arnaud-Haond S, Duarte CM, Serrao EA (2006) Genetic diversity of a clonal angiosperm near its range limit: the case of Cymodocea nodosa at the Canary Islands. Mar Ecol Progr Ser 309:117–129

    Article  CAS  Google Scholar 

  • Bossart JL (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends Ecol Evol 13:202–206

    Article  CAS  Google Scholar 

  • Bouzat JL, Lewin HA, Paige KN (1998) The ghost of genetic diversity past: historical DNA analysis of the greater prairie chicken. Am Nat 152:1–6

    Article  CAS  Google Scholar 

  • Calero CO, Ibanez M, Mayol M, Rosello JA (1998) Random amplified polymorphic DNA (RAPD) marlers detect a single phenotype in Lysimachia minoricensis J.J Rodr. (Primulaceae), a wild extinct plant. Mol Ecol 8:2133–2136

    Article  Google Scholar 

  • Coyer JA, Miller KA, Engle JM, Veldsink J, Cabello-Passini A, Stam WT, Olsen JL (2008) Eelgrass meadows in the California Channel Islands and adjacent coast reveal a mosaic of two species, evidence for introgression and variable clonality. Ann Bot 101:73–87

    Article  CAS  Google Scholar 

  • den Hartog C (1970) The seagrass of the world. North-Holland, Amsterdam

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Duarte CM (2002) The future of seagrass meadows. Environ Conserv 29:192–206

    Article  Google Scholar 

  • Duarte CM, Chiscano CL (1999) Seagrass biomass and production: a reassessment. Aquat Bot 65:159–174

    Article  Google Scholar 

  • Ehlers A, Worm B, Reusch TBH (2008) Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Mar Ecol Prog Ser 355:1–7

    Article  Google Scholar 

  • Erftemeijer PLA, van Beek JKL, Ochieng CA, Jager Z, Los HJ (2008) Eelgrass seed dispersal via floating generative shoots in the Dutch wadden sea: a model approach. Mar Ecol Prog Ser 358:115–124

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA. Genet Soc Amer 131:479–491

    CAS  Google Scholar 

  • Fortes MD (1988) Mangrove and seagrass beds of East Asia: habitats under stress. Ambio 17:207–213

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48:361–372

    Article  CAS  Google Scholar 

  • Guo X, Yanagi T (1996) Seasonal variation of residual current in Tokyo Bay. Jpn Diagn Numer Exp J Oceanogr 52:597–616

    Google Scholar 

  • Harwell MC, Orth RJ (2002) Long-distance dispersal in a marine macrophyte. Ecology 83:3319–3330

    Article  Google Scholar 

  • Hastings A, Harrison S (1994) Metapopulation dynamics and genetics. Ann Rev Ecol Syst 25:167–188

    Article  Google Scholar 

  • Hemminga MA, Duarte CM (2000) Seagrass ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Horiguchi F, Yamamoto J, Nakata K (2001) A numerical simulation of the seasonal cycle of temperature, salinity and velocity fields in Tokyo Bay. Mar Pollut Bull 43:145–153

    Article  CAS  Google Scholar 

  • Hughes AR, Stachowicz JJ (2004) Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. PNAS 101:8998–9002

    Article  CAS  Google Scholar 

  • Izumi S (1908) Fishery map of Tokyo Bay. Ministry of Agriculture and Commerce, Tokyo

    Google Scholar 

  • Jernakoff P, Brearley A, Nielsen J (1996) Factors affecting grazer-epiphyte interactions in temperate seagrass meadows. Oceanogr Mar Biol 34:109–162

    Google Scholar 

  • Kikuchi T, Pérès JM (1980) Consumer ecology of seagrass beds. In: McRoy CP, Helfferich C (eds) Seagrass ecosystems: a scientific perspective. Narcel Dekker, New York, pp 147–193

    Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    Google Scholar 

  • Martin P, Sebastien D, Gilles T, Auby I, Xavier de M, Eric E, Noel C, Viala C (2010) Long-term evolution (1988–2008) of Zostera spp. meadows in Arcachon Bay (Bay of Biscay). Estuar Coast Shelf Sci 87:357–366

    Article  CAS  Google Scholar 

  • Martins PS, Jain SK (1979) Role of genetic variation in the colonizing ability of rose clover (Trifolium hirtum ALL.). Am Nat 114:591–595

    Article  Google Scholar 

  • McRoy CP (1968) The distribution and biogeography of Zostera marina (Eelgrass) in Alaska. Pac Sci 22:507–513

    Google Scholar 

  • Moore KA, Jarvis JC (2008) Environmental factors affecting recent summertime eelgrass diebacks in the Lower Chesapeake Bay: implications for long-term persistence. Coast Res, pp 135–147

  • Muniz-Salazar R, Talbot SL, Sage GK, Ward DH, Cabello-Pasini A (2005) Population genetic structure of annual and perennial populations of Zostera marina L. along the Pacific coast of Baja California and the Gulf of California. Mol Ecol 14:711–722

    Google Scholar 

  • Muniz-Salazar R, Talbot SL, Sage GK, Ward DH, Cabello-Pasini A (2006) Genetic structure of eelgrass Zostera marina meadows in an embayment with restricted water flow. Mar Ecol Progr Ser 309:107–116

    Article  CAS  Google Scholar 

  • Nakase K (2000) Quantitative estimation of eelgrass distribution from the viewpoint of external forces in Takeoka Beach, Tokyo Bay, Japan. Biol Mar Mediterr 7:397–400

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Olsen JL, Stam WT, Coyer JA, Reusch TBH, Billingham M, Bostrom C, Calvert E, Christie H, Granger S, Lumiere RL, Milchakova N, Secq MO, Procaccini G, Sanjabi B, SERRÃO E, Veldsink J, Widdicombe S, Wyllie-Echeverria S (2004) North atlantic phylogeography and large-scale population differentiation of seagrass Zostera marina L. Mol Ecol 13:1923–1941

    Article  CAS  Google Scholar 

  • Omori Y (1993) Zosteraceous species endemic to Japan. Bull Water Plant Soc Jpn 51:19–25

    Google Scholar 

  • Orth RJ, Luckenbach M, Moore KA (1994) Seed dispersal in a marine macrophyte: implications for colonization and restoration. Ecology 75:1927–1939

    Article  Google Scholar 

  • Orth RJ, Carruthers TJB, Dennison WC, Duarte CM, Fourqurean JW, Heck KL Jr, Hughes AR, Olyarnik S, Williams SL, Kendrick GA, Kenworthy WJ, Short FT, Waycott M (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996

    Article  Google Scholar 

  • Pettitt RJ, Mousadik AE, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  Google Scholar 

  • Procaccini G, Mazella L (1998) Population genetic structure and gene flow in the seagrass Posidonia oceanica assessed using microsatellite analysis. Mar Ecol Progr Ser 169:133–141

    Article  Google Scholar 

  • Procaccini G, Olsen JL, Reusch TBH (2007) Contribution of genetics and genomics to seagrass biology and conservation. J Exp Mar Biol Ecol 350:234–259

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP version 1.2: population genetic software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103

    CAS  Google Scholar 

  • Reusch TBH (2000a) A microsatellite-based estimation of clonal diversity and population subdivision in Zostera marina, a marine flowering plant. Mol Ecol 9:127–140

    Article  CAS  Google Scholar 

  • Reusch TBH (2000b) Five microsatellite loci in eelgrass Zostera marina and a test of cross-species amplification in Z. noltii and Z. japonica. Mol Ecol 9:365–378

    Article  Google Scholar 

  • Reusch TBH (2000c) Pollination in marine realm: microsatellites reveal high outcrossing rates and multiple paternity in eelgrass Zostera marina. Heredity 85:459–465

    Article  Google Scholar 

  • Reusch TBH (2001) New markers–old questions: population genetics of seagrasses. Mar Ecol Progr Ser 211:261–274

    Article  CAS  Google Scholar 

  • Reusch TBH (2002) Microsatellite reveal high population connectivity in eelgrass (Zostera marina) in two contrasting coastal areas. Limnol Oceanogr 47:78–85

    Article  Google Scholar 

  • Reusch TBH, Boström C, Stam WT, Olsen JL (1999a) An ancient eelgrass clone in the Baltic. Mar Ecol Progr Ser 183:301–304

    Article  Google Scholar 

  • Reusch TBH, Stam WT, Olsen JL (1999b) Size and estimated age of genets in eelgrass Zostera marina L. assessed with microsatellite markers. Mar Biol 133:519–524

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    Google Scholar 

  • Ruckelshaus MH (1996) Estimation of genetic neighborhood parameters from pollen and seed dispersal in the marine angiosperm Zostera marina L. Evolution 50:856–864

    Article  Google Scholar 

  • Ruckelshaus MH (1998) Spatial scale of genetic structure and an indirect estimate of gene flow in eelgrass, Zostera marina. Evolution 52:330–343

    Article  Google Scholar 

  • Rueda JL, Marina P, Urra J, Salas C (2009) Changes in the composition and structure of a molluscan assemblage due to eelgrass loss in southern Spain (Alboran Sea). J Mar Biol Assoc UK 89:1319–1330

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructuring phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Schenider S, Roessli SD, Excoffier L (2001) Arlequin: a software for population genetics data analysis. Ver 2.001. Genetics and Biometry Lab. Department of Anthropology, University of Geneva, Geneva

    Google Scholar 

  • Shoji Y, Hasegawa K (2004) Distribution of Eelgrass Zostera marina of Coastal Sea Waters in Chiba Prefecture. Bull Chiba Pref Fish Res Cen 3:77–86 (In Japanese)

    Google Scholar 

  • Shorts FT, Wyllie-Echeverria S (1996) Natural and human-induced disturbance in seagrass. Environ Conserv 23:17–27

    Article  Google Scholar 

  • Swofford DL (2001) PAUP* 4.0: phylogenetic analysis using parsimony, beta version 8. Sinauer, Sunderland

    Google Scholar 

  • Tanaka N, Omori Y, Nakaoka M, Aioi K (2002) Gene flow among populations of Zostera caespitosa Miki (Zosteraceae) in Sanriku Coast, Japan. Otsuchi Mar Sci 27:17–22

    Google Scholar 

  • Tanaka N, Shoji Y, Nakaoka M, Ishii M, Lim BK (2006) Distribution of Zostera marina (Zosteraceae) in Coastal Seawaters in the Sagami Sea. Mem Nat Sci Mus Tokyo 42:53–57

    Google Scholar 

  • Tanaka N, Aida S, Akaike S, Aramaki H, Chiyokubo T, Chow S, Fujii A, Fujiwara M, Ikeuchi H, Ishii M, Ishikawa R, Ito H, Kudo T, Muraoka D, Nagahama T, Nambu T, Okumura H, Oshino A, Saigusa M, Shimizu Y, Shoji M, Suwa T, Suzuki K, Takeda K, Tanada N, Tanimoto T, Tsuda F, Urabe S, Yatsuya K, Yoshida G, Yoshimatsu T, Yoshimitsu S, Yoshimura K, Morita K, Saitoh K (2009) Distribution of Zostera species in Japan. I Zostera marina L. (Zosteraceae). Bull Nat Mus Nat Sci Series B (Botany) 35:23–40

  • Unoki S (1985) Tokyo Bay-its physical aspect. In: Oceanography Society of Japan (ed) Coastal oceanography of Japanese Islands. Tokai University Press, Tokyo, pp 344–361

    Google Scholar 

  • van Katwijk MM (2000) Reintroduction of eelgrass (Zostera marina L.) in the Dutch Wadden Sea: a research overview and management vision. In: Wolff WJ, Essink K, Kellermann A, van Leeuwe MA (eds) Challenges to the Wadden Sea. Proceedings of the 10th international scientific Wadden Sea symposium, Groningen, 2000. Ministry of Agriculture, Nature Management and Fisheries/University of Groningen, Department of Marine Biology

  • Waycott M (1998) Genetic variation, its assessment and implications to the conservation of seagrass. Mol Ecol 7:793–800

    Article  Google Scholar 

  • Waycott M, Procaccini G, Les DH, Reusch TBH (2006) Seagrass evolution, ecology and conservation: a genetic perspective. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht

    Google Scholar 

  • Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean WJ, Heck KL Jr, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. PNAS 106:12377–12381

    Article  CAS  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whitlock SL (1999) Indirect measures of gene flow and migration. Heredity 82:117–125

    Article  Google Scholar 

  • Williams SL (2001) Reduced genetic diversity in eelgrass transplantations affects both population growth and individual fitness. Ecol Appl 11:1472–1488

    Article  Google Scholar 

  • Williams SL, Heck KL (2001) Seagrass community ecology. In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, pp 317–337

    Google Scholar 

  • Yamakita T, Nakaoka M, Kondo A, Ishi M, Shoji Y (2005) Long-term spatial dynamics of a seagrass bed on the Futtsu tidal flat in Tokyo Bay, Japan. Jpn J Conserv Ecol 10:129–138

    Google Scholar 

  • Zimmerman RC, Reguzzoni JL, Alberte RS (1995) Ealgarass (Zostera marina L.) transplants in San Francisco Bay: Role of light availability on metabolism, growth and survival. Aquat Bot 51:67–86

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Yuji Omori, Takahiro Kudo, Futtsu Fishery Cooperative for collecting samples, and Toshiyuki Yamaguchi, Yasuyuki Watano, Tadashi Kajita for helpful comments to analyze the data. Thanks also to Chikako Ishii and Haruka Matsuyoshi for technical support of genetic analysis and Shoh Nagata and Yuki Ando for making figures.

Author information

Authors and Affiliations

  1. Tsukuba Botanical Garden, National Museum of Nature and Science, 4-1-1, Amakubo, Tsukuba, Ibaraki, 305-0005, Japan

    Norio Tanaka

  2. Graduate School of Science, Chiba University, 1-33, Yayoicho, Inage, Chiba, 263-8522, Japan

    Teruko Demise

  3. Chiba Prefectural Fisheries Research Center, 2492, Kotsubo, Futtsu, Chiba, 293-0042, Japan

    Mitsuhiro Ishii & Yasumasa Shoji

  4. Akkeshi Marine Station, Field Science Center for Northern Biosphere, Hokkaido University, Aikappu, Akkeshi, Hokkaido, 088-1113, Japan

    Masahiro Nakaoka

Authors
  1. Norio Tanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Teruko Demise
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mitsuhiro Ishii
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yasumasa Shoji
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masahiro Nakaoka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Norio Tanaka.

Additional information

Communicated by T. Reusch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tanaka, N., Demise, T., Ishii, M. et al. Genetic structure and gene flow of eelgrass Zostera marina populations in Tokyo Bay, Japan: implications for their restoration. Mar Biol 158, 871–882 (2011). https://doi.org/10.1007/s00227-010-1614-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-010-1614-2

Keywords

Search

Navigation