Skip to main content

Advertisement

Log in

Responses to salinity of Spartina hybrids formed in San Francisco Bay, California (S. alterniflora × foliosa and S. densiflora × foliosa )

  • Invasive Spartina
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

San Francisco Bay (SFB), which supports large populations of the California native cordgrass Spartina foliosa, has been the recipient of introductions of S. alterniflora and S. densiflora. Hybrids have arisen between the native and these exotic species. Sterile F1 S. densiflora × foliosa hybrids have formed numerous times in a number of marshes, while introgressing S. alterniflora × foliosa hybrids are fully fertile and invaded widely in SFB, especially onto naturally-open low tidal flats by inundation-tolerant hybrids. Sarcocornia pacifica, pickleweed, dominates the mid-to-upper marsh zones where the hypersaline conditions that occur during the summer drought, characteristic of this climate, exclude S. foliosa. Here we report on two glasshouse experiments investigating the salinity tolerance of hybrid Spartina. Some hybrids of both origins grew well and flowered at high salinity levels while the parental species grew little and did not flower. Our results imply that mid-zone marshes are also vulnerable to invasion by salinity-tolerant Spartina hybrids. Herbicide control implemented over the last 10 years targeting both the exotic species and their hybrids have reduced their extent. However, efforts in monitoring and management of exotic Spartina and its hybrids must continue as vast areas of tidal marsh restoration are underway and planned in SFB; colonization by Spartina hybrids tolerant to inundation and/or salinity will greatly alter restoration trajectories. These concerns are all the more vital given projections of climate change and its effects on salinity and sea level rise in SFB salt marshes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

GCC:

Global climate change

ISP:

Invasive Spartina Project

ppt:

Parts per thousand

S. axf :

Spartina alterniflora × foliosa

S. dxf :

Spartina densiflora × foliosa

SFB:

San Francisco Bay

SLR:

Sea level rise

References

  • Abbas AM, Rubio-Casal AE, De Cires A, Figuero ME, Lambert AM, Castillo JM (2012) Effects of flooding on germination and establishment of the invasive cordgrass Spartina densiflora. Weed Res 52:269–276

    Article  Google Scholar 

  • Ainouche ML, Fortune PM, Salmon A, Parisod C, Grandbastien MA et al (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biol Invasions 11:1159–1173

    Article  Google Scholar 

  • Alberti J, Méndez CA, Daleo P, Fanjul E, Silliman BR, Bertness M (2010) Abiotic stress mediates top-down and bottom-up control in a Southwestern Atlantic salt marsh. Oecologia 163:181–191

    Article  PubMed  Google Scholar 

  • Anttila CK, Daehler CC, Rank NE, Strong DR (1998) Greater male fitness of a rare invader (Spartina alterniflora, Poaceae) threatens a common native (Spartina foliosa) with hybridization. Am J Bot 85:1597–1601

    Article  CAS  PubMed  Google Scholar 

  • Ayres DA, Strong DR (2010) Hybrid cordgrass (Spartina) and tidal marsh restoration in San Francisco Bay: if you build it, they will come. In: Ayres DR, Kerr DW, Ericson SD, Olofson PR (eds) Proceedings of the Third international conference on invasive Spartina, 2004. San Francisco Estuary Invasive Spartina Project of the California State Coastal Conservancy, Oakland, pp 125–126

    Google Scholar 

  • 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 8:1179–1186

    Article  Google Scholar 

  • Ayres DR, Strong DR, Baye P (2003) Spartina foliosa—a common species on the road to rarity? Madroño 50:209–213

    Google Scholar 

  • 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. Biol Invasions 6:221–231

    Article  Google Scholar 

  • Ayres DR, Grotkopp E, Zaremba K, Sloop CM, Blum MJ, Bailey JP, Anttila CK, Strong DR (2008a) Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. Am J Bot 95(6):713–719

    Article  PubMed  Google Scholar 

  • Ayres DA, Zaremba K, Sloop CM, Strong DR (2008b) Sexual reproduction of cordgrass hybrids (Spartina foliosa × alterniflora) invading tidal marshes in San Francisco Bay. Divers Distrib 14:187–195

    Article  Google Scholar 

  • Blum MJ, Bando KJ, Katz M, Strong DR (2007) Geographic structure, genetic diversity and source tracking of Spartina alterniflora. J Biogeogr 34:2055–2069

    Article  Google Scholar 

  • Cain DJ, Harvey HT (1983) Evidence of salinity-induced ecophenic variation in cordgrass (Spartina foliosa Trin.). Madroño 30(1):50–62

    Google Scholar 

  • Callaway JC, Parker VT, Vasey MC, Schile LM (2007) Emerging issues for the restoration of tidal marsh ecosystems in the context of predicted climate change. Madrono 54(3):234–248

    Article  Google Scholar 

  • Capitol News (2014) http://www.capitalpress.com/stories-of-the-week/20141114/delta-tunnels-the-next-big-water-fight-in-calif. Accessed 20 January 2015

  • Castillo JM, Fernandez-Baco L, Castellanos EM, Luque CJ, Figueroa ME, Davy AJ (2000) Lower limits of Spartina densiflora and S. maritima in a Mediterranean salt marsh determined by different ecophysiological tolerances. J Ecol 88(5):801–812

    Article  Google Scholar 

  • Castillo JM, Mateos-Naranjo E, Nieva FJ, Figueroa E (2008) Plant zonation at salt marshes of the endangered cordgrass Spartina maritima invaded by Spartina densiflora. Hydrobiologia 614:363–371

    Article  Google Scholar 

  • Castillo JM, Ayres DR, Leira-Doce P, Bailey J, Blum M, Strong DR, Luque T, Figueroa E (2010) The production of hybrids with high ecological amplitude between exotic Spartina densiflora and native S. maritima in the Iberian Peninsula. Divers Distrib 16:547–558

    Article  Google Scholar 

  • Castillo JM, Grewell BJ, Pickart A, Bortolus A, Peña C, Figueroa E, Sytsma M (2014) Phenotypic plasticity of invasive Spartina densiflora (Poaceae) along a broad latitudinal gradient on the Pacific Coast of North America. Am J Bot 101:448–458

    Article  PubMed  Google Scholar 

  • Chelaifa H, Monnier A, Ainouche M (2010) Transcriptomic changes following recent natural hybridization and allopolyploidy in the salt marsh species Spartina × townsendii and Spartina anglica (Poaceae). New Phytol 186:161–174

    Article  CAS  PubMed  Google Scholar 

  • Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558

    Article  CAS  PubMed  Google Scholar 

  • Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    Article  CAS  PubMed  Google Scholar 

  • Daehler CC, Strong DR (1996) Status, prediction and prevention of introduced cordgrass Spartina spp. invasions in Pacific estuaries, USA. Biol Conserv 78:51–58

    Article  Google Scholar 

  • Daehler CC, Antilla CK, Ayres DR, Strong DR, Bailey JP (1999) Evolution of a new ecotype of Spartina alterniflora (Poaceae) in San Francisco Bay, California, USA. Am J Bot 86:543–546

    Article  CAS  PubMed  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci 97(13):7043–7050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faber PM (2000) Good intentions gone awry. Calif Coast Ocean 16:14–17

    Google Scholar 

  • Fortune PM, Schierenbeck K, Ayres DR, Bortolus A, Catrice O, Brown S, Ainouche ML (2008) The enigmatic invasive Spartina densiflora: a history of hybridizations in a polyploidy context. Mol Ecol 17:4304–4316

    Article  CAS  PubMed  Google Scholar 

  • Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17(1):22–27

    Article  Google Scholar 

  • Hacker SD, Heimer D, Hellquist CE, Reeder TG, Reeves B, Riordan T, Dethier MN (2001) A marine plant (Spartina anglica) invades widely varying habitats: potential mechanism of invasion and control. Biol Invasions 3:211–217

    Article  Google Scholar 

  • Hall RJ, Hastings A, Ayres DR (2006) Explaining the explosion: modelling a hybrid invasion. Proc R Soc B 273:1385–1389

    Article  PubMed  PubMed Central  Google Scholar 

  • Hester MW, Mendelssohn IA, McKee KL (1998) Intraspecific variation in salt tolerance and morphology in Panicum hemitomon and Spartina alterniflora (Poaceae). Int J Plant Sci 159(1):127–138

    Article  Google Scholar 

  • Hester MW, Mendelssohn IA, McKee KL (2001) Species and population variation to salinity stress in Panicum hemitomon, Spartina patens, and Spartina alterniflora: morphological and physiological constraints. Environ Exp Bot 46:277–297

    Article  CAS  Google Scholar 

  • Hinde HP (1954) The vertical distribution of salt marsh phanerogams in relation to tide levels. Ecol Monogr 24:209–225

    Article  Google Scholar 

  • Hogle I (2011) San Francisco estuary invasive Spartina Project 2008–2009 Monitoring Report, ed. SFEISP State Coastal Conservancy, 1330 Broadway, 13th Floor, Oakland, CA 94612. Oakland CA. http://www.spartina.org/project_documents/2008-09_MonReport_ALLwCover.pdf

  • Hovick SM, Whitney KD (2014) Hybridisation is associated with increased fecundity and size in invasive taxa: meta-analytic support for the hybridization invasion hypothesis. Ecol Lett 17:1464–1477

    Article  PubMed  PubMed Central  Google Scholar 

  • Idaszkin YL, Bortolus A, Bouza PJ (2014) Flooding effect on the distribution of native austral cordgrass Spartina densiflora in Patagonian salm marshes. J Coast Res 30:59–62

    Article  Google Scholar 

  • Janousek CN, Folger CL (2014) Variation in tidal wetland plant diversity and composition within and among coastal estuaries: assessing the relative importance of environmental gradients. J Veg Sci 25:534–545

    Article  Google Scholar 

  • Josselyn M (1983) The ecology of San Francisco Bay tidal marshes: a community profile. US Fish and Wildlife Service, Division of Biological Services, Washington

    Google Scholar 

  • Kittelson PM, Boyd MJ (1997) Mechanisms of expansion for an introduced species of cordgrass, Spartina densiflora, in Humboldt Bay, California. Estuaries 20:770–778

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Mahall BE, Park RB (1976a) The ecotone between Spartina foliosa Trin. and Salicornia virginica L. in salt marshes of northern San Francisco Bay II. Soil water and salinity. J Ecol 64:793–809

    Article  Google Scholar 

  • Mahall BE, Park RB (1976b) The ecotone between Spartina foliosa Trin. and Salicornia virginica L. in salt marshes of northern San Francisco Bay III. Soil aeration and tidal immersion. J Ecol 64:811–819

    Article  Google Scholar 

  • Mateos-Naranjo E, Redondo-Gomez S, Luque CL, Castellanos EM, Davy AJ, Figueroa ME (2008) Environmental limitations on recruitment from seed in invasive Spartina densiflora on a southern European salt marsh. Estuar Coast Shelf Sci 79:727–732

    Article  Google Scholar 

  • Mendelssohn IA, Morris JT (2000) Eco-physiological controls on the productivity of Spartina alterniflora Loisel. In: Weinstein MP, Kreeger DA (eds) Concepts and controversies in tidal marsh ecology. Kluwer, Norwell, MA, pp 59–79

    Google Scholar 

  • Nestler J (1977) Interstitial salinity as a cause of ecophenic variation in Spartina alterniflora. Estuar Coast Mar Shelf Sci 5:707–714

    Article  Google Scholar 

  • Nieva FJJ, Díaz-Espejo A, Castellanos EM, Figueroa ME (2001) Field variability of invading populations of Spartina densiflora Brong. In different habitats of the Odiel Marshes (SW Spain). Estuar Coast Shelf Sci 52:515–527

    Article  CAS  Google Scholar 

  • Nieva FJJ, Castillo JM, Luque CJ, Figueroa ME (2003) Ecophysiology of tidal and non-tidal populations of the invading cordgrass Spartina densiflora; seasonal and diurnal patterns in a Mediterranean climate. Estuar Coast Shelf Sci 57:919–928

    Article  CAS  Google Scholar 

  • Olofson Environmental Inc. and San Francisco Estuary Invasive Spartina Project (2013) San Francisco Estuary Invasive Spartina Project Revegetation Program: 2012–2013 Installation Report and 2013–2014 Revegetation Plan, ed. SFEISP State Coast. Conserv. Oakland, CA. http://www.spartina.org/documents/ISPRevegetation_2012-2013-2014_Final_111913_sm_000.pdf

  • Pennings SC, Callaway RM (1992) Salt marsh zonation: the relative importance of competition and physical factors. Ecology 73:681–690

    Article  Google Scholar 

  • Pennings SC, Grant M-B, Bertness MD (2005) Plant zonation in low-latitude salt marshes: disentangling the roles of flooding, salinity and competition. J Ecol 93:159–167

    Article  Google Scholar 

  • Pezeshiki SR, DeLaune RD (1995) Variation in response of two U.S. Gulf Coast populations of Spartina alterniflora to hypersalinity. J Coast Res 11:89–95

    Google Scholar 

  • Proffitt CE, Chiasson RL, Owens AB, Edwards KR, Travis SR (2005) Spartina alterniflora genotype influences facilitation and suppression of high marsh species colonizing an early successional marsh. J Ecol 93:404–416

    Article  Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation and speciation. Heredity 83:363–372

    Article  PubMed  Google Scholar 

  • Rohmer T, Kerr D, Hogle I (2014) San Francisco Estuary Invasive Spartina Project 2012 ISP Monitoring and Treatment Report, ed. SFEISP State Coastal Conservancy, 1330 Broadway, 13th Floor, Oakland, CA 94612. Oakland CA. http://www.spartina.org/documents/

  • Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14:1163–1175

    Article  CAS  PubMed  Google Scholar 

  • Seliskar DM (1995) Exploiting plant genetic diversity for coastal salt marsh creation and restoration. In: Khan MA, Ungar IA (eds) Biology of salt tolerant plants. Department of Botany, University of Karachi, Karachi, pp 407–416

    Google Scholar 

  • Sloop CM, Ayres DR, Strong DR (2010) The rapid evolution of self-fertility in Spartina hybrids (S. alterniflora × foliosa) invading San Francisco Bay, CA. Biol Invasions 11:1131–1144

    Article  Google Scholar 

  • Spicher D, Josselyn M (1985) Spartina (Gramineae) in Northern California: distribution and taxonomic notes. Madroño 32:158–167

    Google Scholar 

  • Strong DR, Ayres DA (2016) Control and consequences of Spartina spp. invasions with focus upon San Francisco Bay. Biol Inv. doi:10.1007/s10530-015-0980-6

  • Strong DR, Ayres DR (2013) Ecological and evolutionary misadventures of Spartina. Annu Rev Ecol Evol Syst 44:389–410

    Article  Google Scholar 

  • Thorne KM, Takekawa JY, Elliott-Fisk DL (2012) Ecological effects of climate change on salt marsh wildlife: a case study from a highly urbanized estuary. J Coast Res 28(6):1477–1487

    Article  Google Scholar 

  • Thorne KM, Elliott-Fisk DL, Wylie GD, Perry WM, Takekawa JY (2014) Importance of biogeomorphic and spatial properties in assessing a tidal salt marsh vulnerability to sea-level rise. Estuar Coasts 37:941–951

    Article  CAS  Google Scholar 

  • Trnka S, Zedler JB (2000) Site conditions, not parental phenotype, determine the height of Spartina foliosa. Estuaries 23(4):572–582

    Article  Google Scholar 

  • Watson EB, Bryne R (2012) Recent (1975–2004) vegetation change in the San Francisco Estuary, California, tidal marshes. J Coast Res 28(1):51–63

    Article  Google Scholar 

Download references

Acknowledgments

We thank Krista Hoffman and Pablo Rosso for their contributions to this project, two anonymous reviewers, and the UC Davis Spartina Lab for their support. This research was funded by California Sea Grant #27CN to DRS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Debra R. Ayres.

Additional information

Guest editors: Alan Gray and Malika Ainouche/Invasive Spartina.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, A.K., Ayres, D.R., Pakenham-Walsh, M.R. et al. Responses to salinity of Spartina hybrids formed in San Francisco Bay, California (S. alterniflora × foliosa and S. densiflora × foliosa ) . Biol Invasions 18, 2207–2219 (2016). https://doi.org/10.1007/s10530-015-1011-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-1011-3

Keywords

Navigation