Biological Invasions

, Volume 18, Issue 8, pp 2267–2281 | Cite as

Changes in the population genetics of an invasive Spartina after 10 years of management

  • Brian S. OrtEmail author
  • Whitney J. Thornton


Spartina foliosa is native to the San Francisco, California, Bay and Estuary. Spartina alterniflora was introduced to the Bay in the 1970s and subsequently hybridized with S. foliosa. Backcrossing created an invasive hybrid swarm able to outcompete S. foliosa within its tidal range and spread into higher and lower intertidal zones, drastically altering ecological communities. The San Francisco Estuary Invasive Spartina Project (ISP) has implemented a treatment program that has reduced the net area of invasive Spartina by 96 % from its peak of 323 hectares. An endangered bird, the California Ridgway’s Rail, takes advantage of habitat characteristics supplied by hybrid Spartina, prompting treatment restrictions in some marshes to preserve hybrid Spartina for the benefit of rails. We investigated changes in the population genetics of the invasion after 10 years of eradication efforts and after three subsequent years without eradication in some locations. Our investigation covered three areas: sites surrounding and including the restricted treatment marshes; sites in the southern Bay similar to proposed salt pond restoration projects; and samples collected Baywide. Our results support previous descriptions of a system of self-fertile hybrid plants that supply seed for mostly localized recruitment into available habitat. Compared to published work from 2003 to 2004, before large-scale eradication efforts began, genetic diversity has generally declined and inbreeding within hybrid populations has increased during and after the period of treatment by the ISP. These observations are perhaps due to pollen limitation as a result of the elimination of most hybrid plants by the ISP. We did not detect strong population genetic boundaries Baywide, but a genetically distinguishable localized introduction was detected in 10 of 11 Bay regions, suggesting leptokurtic dispersal. The restricted treatment areas may allow for continued introgression with S. foliosa, recolonization, and longer persistence of these invasive plants in the San Francisco Bay. Proximity to hybrid Spartina threatens the success of major restoration projects.


Spartina foliosa Spartina alterniflora San Francisco Estuary Population genetics Hybridization 



We are very grateful to the California State Coastal Conservancy for their commitment to manage and fund the San Francisco Estuary Invasive Spartina Project. Data in this paper was collected under the auspices of the ISP. The ISP has received funding from: California State Coastal Conservancy, State Wildlife Conservation Board, CALFED Bay Delta Program, US Fish and Wildlife Service, American Reinvestment and Recovery Act through National Oceanic and Atmospheric Administration, U.S. Environmental Protection Agency, Gordon and Betty Moore Foundation, David and Lucile Packard Foundation, S. D. Bechtel Jr. Foundation, North American Wetlands Conservation Act and National Coastal Wetlands Conservation Grant Program. We thank Ingrid Hogle for GIS expertise and Simon Gunner for help with the experiments on new recruits, and the rest of our co-workers, partners, grantees and contractors, too numerous to name, past and present, for their invaluable contributions to the ISP’s regional coordination, mapping, treatment and revegetation efforts. The comments of two anonymous reviewers and the editors of this special issue greatly improved the manuscript, and we thank them for their efforts. We thank the organizers of the 4th International Conference on Invasive Spartina in Rennes, France (July 2014), and the editors for inviting manuscripts inspired by the conference.

Compliance with ethical standards

The San Francisco Estuary Invasive Spartina Project is funded by the California State Coastal Conservancy. The authors are employees of Olofson Environmental, Inc., which receives funding from the Conservancy.

Supplementary material

10530_2016_1177_MOESM1_ESM.pdf (5.4 mb)
Supplementary material 1 (PDF 5516 kb)


  1. Ainouche ML, Fortune PM, Salmon A, Parisod C, Grandbastien MA, Fukunaga K, Ricou M, Misset MT (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biol Invasions 11:1159–1173CrossRefGoogle Scholar
  2. Anttila CK, King RA, Ferris C, Ayres DR, Strong DR (2000) Reciprocal hybrid formation of Spartina in San Francisco Bay. Mol Ecol 9:765–770CrossRefPubMedGoogle Scholar
  3. Ayres DR, Strong DR (2010) Hybrid cordgrass (Spartina) and tidal marsh restoration in San Francisco Bay: if you build it, they will come. In: Ayres D, Kerr D, Ericson S, Olofson P (eds) Proceedings of the Third International Conference on Invasive Spartina, 2004 Nov 8–10, San Francisco, CA, USA. San Francisco Estuary Invasive Spartina Project of the California State Coastal Conservancy, Oakland, CAGoogle Scholar
  4. Ayres DR, Garcia-Rossi D, Davis HG, Strong DR (1999) Extent and degree of hybridization between exotic (Spartina alterniflora) and native (S. foliosa) cordgrass (Poaceae) in California, USA determined by random amplified polymorphic DNA (RAPDs). Mol Ecol 8:1179–1186CrossRefGoogle Scholar
  5. Ayres DR, Smith DL, Zaremba K, Klohr S, Strong DR (2004) Spread of exotic cordgrasses and hybrids (Spartina sp.) in the tidal marshes of San Francisco Bay, California, USA. Biol Invasions 6:221–231CrossRefGoogle Scholar
  6. Ayres DR, Grotkopp E, Zaremba K, Sloop CM, Blum MJ, Bailey JP, Anttila CK, Strong DR (2008) Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. Am J Bot 95:713–719CrossRefPubMedGoogle Scholar
  7. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, Laboratoire Génome, Populations. Université de Montpellier II: MontpellierGoogle Scholar
  8. Blum MJ, Sloop CM, Ayres DR, Strong DR (2004) Characterization of microsatellite loci in Spartina species (Poaceae). Mol Ecol Notes 4:39–42CrossRefGoogle Scholar
  9. Blum MJ, Bando KJ, Katz M, Strong DR (2007) Geographic structure, genetic diversity and source tracking of Spartina alterniflora. J Biogeogr 34:2055–2069CrossRefGoogle Scholar
  10. Callaway JC, Josselyn MN (1992) The introduction and spread of smooth cordgrass (Spartina alterniflora) in South San Francisco Bay. Estuaries 15:218–226CrossRefGoogle Scholar
  11. Daehler CC, Strong DR (1997) Hybridization between introduced smooth cordgrass (Spartina alterniflora; Poaceae) and native California cordgrass (S. foliosa) in San Francisco Bay, California, USA. Am J Bot 84:607–611CrossRefPubMedGoogle Scholar
  12. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci 97:7043–7050CrossRefPubMedPubMedCentralGoogle Scholar
  13. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  14. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  15. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  16. Faber P (2000) Grass wars—good intentions gone awry. Why would anyone bring an alien cordgrass into S.F. Bay? Calif Coast Ocean 16:14–17Google Scholar
  17. Goals Project (1999) Baylands ecosystem habitat goals. In: Olofson P (ed) A report of habitat recommendations prepared by the San Francisco Bay Area Wetlands Ecosystem Goals Project. U.S. Environmental Protection Agency, San Francisco, CA/San Francisco Bay Regional Water Quality Board, Oakland, CAGoogle Scholar
  18. Goals Project (2015) The baylands and climate change: what we can do. In: Olofson P (ed) Baylands ecosystem habitat goals science update 2015 prepared by the San Francisco Bay Area Wetlands Ecosystem Goals Project. California State Coastal Conservancy, Oakland, CAGoogle Scholar
  19. Grosholz ED, Levin LA, Tyler AC, Neira C (2009) Changes in community structure and ecosystem function following Spartina alterniflora invasion of Pacific estuaries. In: Silliman BR, Grosholz ED, Bertness MD (eds) Human impacts on salt marshes: a global perspective. University of California Press, Berkeley, pp 23–40Google Scholar
  20. Hall RJ, Hastings A, Ayres DR (2006) Explaining the explosion: modelling hybrid invasions. Proc R Soc B Biol Sci 273:1385–1389CrossRefGoogle Scholar
  21. Hughes AR, Lotterhos KE (2014) Genotypic diversity at multiple spatial scales in the foundation marsh species, Spartina alterniflora. Mar Ecol Prog Ser 497:105–117CrossRefGoogle Scholar
  22. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedPubMedCentralGoogle Scholar
  23. Olofson Environmental Inc. (2012) San Francisco Estuary Invasive Spartina Project California clapper rail habitat enhancement restoration and monitoring plan. Prepared for the California State Coastal Conservancy San Francisco Invasive Spartina Project, 1330 Broadway, 13th Floor, Oakland, CA 94612, p 94Google Scholar
  24. Overton CT, Casazza ML, Takekawa JY, Strong DR, Holyoak M (2014) Tidal and seasonal effects on survival rates of the endangered California clapper rail: does invasive Spartina facilitate greater survival in a dynamic environment? Biol Invasions 16:1897–1914CrossRefGoogle Scholar
  25. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  26. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  27. Regan TJ, McCarthy MA, Baxter PWJ, Dane Panetta F, Possingham HP (2006) Optimal eradication: when to stop looking for an invasive plant. Ecol Lett 9:759–766CrossRefPubMedGoogle Scholar
  28. Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372CrossRefPubMedGoogle Scholar
  29. Rohmer T, Kerr D, Hogle I (2014) San Francisco Estuary Invasive Spartina Project 2012 ISP monitoring and treatment report. Prepared for the California State Coastal Conservancy San Francisco Invasive Spartina Project, 1330 Broadway, 13th Floor, Oakland, CA 94612, p 86Google Scholar
  30. Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  31. Schierenbeck KA, Ellstrand NC (2008) Hybridization and the evolution of invasiveness in plants and other organisms. Biol Invasions 11:1093–1105CrossRefGoogle Scholar
  32. Sloop CM, Ayres DR, Strong DR (2009) The rapid evolution of self-fertility in Spartina hybrids (Spartina alterniflora × foliosa) invading San Francisco Bay, CA. Biol Invasions 11:1131–1144CrossRefGoogle Scholar
  33. Sloop CM, Ayres DR, Strong DR (2011) Spatial and temporal genetic structure in a hybrid cordgrass invasion. Heredity 106:547–556CrossRefPubMedGoogle Scholar
  34. Sloop CM, McGray HG, Blum MJ, Strong DR (2005) Characterization of 24 additional microsatellite loci in Spartina species (Poaceae). Conserv Genet 6:1049–1052CrossRefGoogle Scholar
  35. Strong D, Ayres D (2009) Spartina introductions and consequences in salt marshes. In: Silliman Brian R, Grosholz E, Bertness MD (eds) Human impacts on salt marshes: a global perspective. University of California Press Ltd, LondonGoogle Scholar
  36. Strong DR, Ayres DR (2013) Ecological and evolutionary misadventures of Spartina. Annu Rev Ecol Evol Syst 44:389–410CrossRefGoogle Scholar
  37. Thornton W, Gunner S, Ort B (2013) Is restoration of salt marshes enhanced by proximity to established native Spartina?. State of the Estuary, OaklandGoogle Scholar
  38. US Army Corps of Engineers (1978) Pre-construction report. Shoreline Erosion Control Demonstration Project, Alameda, CAGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Olofson Environmental, Inc.San Francisco Estuary Invasive Spartina ProjectOaklandUSA

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