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Biological Invasions

, Volume 18, Issue 8, pp 2175–2187 | Cite as

Phenotypic plasticity and population differentiation in response to salinity in the invasive cordgrass Spartina densiflora

  • Brenda J. GrewellEmail author
  • Jesús M. Castillo
  • Meghan J. Skaer Thomason
  • Rebecca E. Drenovsky
Invasive Spartina

Abstract

Salinity and tidal inundation induce physiological stress in vascular plant species and influence their distribution and productivity in estuarine wetlands. Climate change-induced sea level rise may magnify these abiotic stressors and the physiological stresses they can cause. Understanding the potential of invasive plants to respond to predicted salinity increases will elucidate their potential niche breadth. To examine potential phenotypic plasticity and functional trait responses to salinity stress in the invasive cordgrass Spartina densiflora, we collected rhizomes from four invasive populations occurring from California to Vancouver Island, British Columbia on the Pacific Coast of North America. In a glasshouse common garden experiment, we measured plant traits associated with growth and allocation, photosynthesis, leaf pigments, and leaf chemistry and calculated plasticity indices across imposed salinity treatments. Fifteen of 21 leaf chemistry, pigment, morphological and physiological traits expressed plastic responses to salinity. When averaged across all measured traits, degree of plasticity did not vary among sampled populations. However, differences in plasticity among populations in response to salinity were observed for 9 of 21 measured plant traits. Leaf chemistry and adaxial leaf rolling trait responses demonstrated the highest degree of plasticity, while growth and allocation measures were less plastic. Phenotypic plasticity of leaf functional traits to salinity indicates the potential of S. densiflora to maintain invasive growth in response to rising estuarine salinity with climate change.

Keywords

Invasive species Phenotypic plasticity Plant invasions Plant functional traits Halophyte Sea level rise 

Notes

Acknowledgments

We thank A. Pickart for encouraging this research. We thank C.J. Futrell who contributed to propagation and maintenance of plant cultures, participated in measurement of plant response traits, and performed chemical analyses of plant tissue. Kevin Rice provided a pressure bomb instrument and comments that improved the manuscript. A. Pickart and A. Bortulus participated in field collection of plant material, and A. Pickart and M. Sytsma provided logistical support.

Supplementary material

10530_2015_1041_MOESM1_ESM.pdf (143 kb)
Supplementary material 1 (PDF 143 kb)

References

  1. Abbas AM, Lambert AM, Rubio-Casal AE, de Cires A, Figueroa E, Castillo JM (2015) Competition from native hydrophytes reduces establishment and growth of invasive dense-flowered cordgrass (Spartina densiflora). PeerJ 3:e1260. doi: 10.7717/peerj.1260 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Adam P (1993) Saltmarsh ecology. Cambridge University Press, CambridgeGoogle Scholar
  3. Ainouche ML, Jenczewski E (2010) Focus on polyploidy. New Phytol 186:1–4CrossRefPubMedGoogle Scholar
  4. Ainouche ML, Baumel A, Salmon A (2004) Spartina anglica C. E. Hubbard: a natural model system for analysing early evolutionary changes that affect allopolyploid genomes. Biol J Linn Soc 82:475–484CrossRefGoogle Scholar
  5. Ainouche ML, Fortune M, Salmon A et al (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biol Invasions 11:1159–1173CrossRefGoogle Scholar
  6. Ainouche ML, Chelaifa J, Ferreira S, Bellot A, Ainouche A, Salmon A (2012) Polyploid evolution in Spartina: dealing with highly redundant hybrid genomes. In: Soltis PS, Soltis DE (eds) Polyploidy and genome evolution. Springer, Berlin, pp 225–243Google Scholar
  7. 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, CA, USA. Biol Invasions 6:221–231CrossRefGoogle Scholar
  8. Ayres DR, Grotkopp EK, Zaremba K et al (2008) Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. Am J Bot 95:713–719CrossRefPubMedGoogle Scholar
  9. Barbour MG (1970) Is any angiosperm an obligate halophyte? Am Midl Nat 84:105–120CrossRefGoogle Scholar
  10. Bates LS, Waldren RP, Teare JD (1973) Rapid determination of free proline for water stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  11. Bertness MD (1991) Zonation of Spartina patens and Spartina alterniflora in a New England salt marsh. Ecology 72:138–148CrossRefGoogle Scholar
  12. Bortolus A (2006) The austral cordgrass Spartina densiflora Brong.: its taxonomy, biogeography and natural history. J Biogeogr 33:158–168CrossRefGoogle Scholar
  13. Callaway JC, Borde AB, Diefenderfer HL, Parker VT, Rybczyk JM, Thom RM (2012) Pacific coast tidal wetlands. In: Batzer DB, Baldwin AH (eds) Wetland habitats of North America: ecology and conservation concerns. University of California Press, Berkeley, pp 103–116Google Scholar
  14. Caño L, Escarré J, Fleck I, Blanco-Moreno JM, Sans FX (2008) Increased fitness and plasticity of an invasive species in its introduced range: a study using Senecio pterophorus. J Ecol 96:468–476CrossRefGoogle Scholar
  15. Castillo JM, Rubio-Casal AE, Redondo S, Antonio A, Alvarez-Lopez A, Luque T, Luque C, Nieva FJ, Castellanos EM, Figueroa ME (2005) Short term responses to salinity of an invasive cordgrass. Biol Invasions 7:29–35CrossRefGoogle Scholar
  16. Castillo JM, Ayres DR, Leira-Doce P, Bailey J, Blum M et al (2010) The production of hydrids with high ecological amplitude between exotic Spartina densiflora and native S. maritima in the Iberian Peninsula. Divers Distrib 16:547–558CrossRefGoogle Scholar
  17. Castillo JM, Grewell BJ, Pickart A, Bortolus A, Peña C, Figueroa E, Sytsma M (2014) Phenotypic plasticity of invasive Spartina densiflora (Poaceae) along the Pacific Coast of North America. Am J Bot 101:1–11CrossRefGoogle Scholar
  18. Castillo JM, Grewell BJ, Pickart AJ, Figueroa E, Sytsma M (2015) Variation in tussock architecture of the invasive cordgrass Spartina densiflora along the Pacific Coast of North America. Biol Invasions. doi: 10.1007/s10530-015-0991-3
  19. Christman MA, James JJ, Drenovsky RE, Richards JH (2009) Environmental stress and genetics influence night-time leaf conductance in the C4 grass Distichlis spicata. Funct Plant Biol 36:50–55CrossRefGoogle Scholar
  20. D’Hertefeldt TD, Eneström JM, Pettresson LB (2014) Geographic and habitat origin influence biomass production and storage translocation in the clonal plant Aegopodium podagraria. PLoS ONE 9:1–8Google Scholar
  21. Di Bella CE, Striker GG, Escaray FJ, Lattanzi FA, Rodriguez AM, Grimaldi AA (2014) Saline tidal flooding effects on Spartina densiflora plants from different positions in the salt marsh. Diversities and similarities on growth, anatomical and physiological responses. Environ Exp Bot 102:27–36CrossRefGoogle Scholar
  22. Dlugosch KM, Parker IM (2008) Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks. Ecol Lett 11:701–709CrossRefPubMedGoogle Scholar
  23. Drenovsky RD, Grewell BJ, D’Antonio CM, Funk JL, James JJ, Molinari N, Parker IM, Richards CL (2012) A functional trait perspective on plant invasion. Ann Bot Lond 110:141–153CrossRefGoogle Scholar
  24. Duarte B, Sleimi N, Caçador I (2014) Biophysical and biochemical constraints imposed by salt stress: learning from halophytes. Front Plant Sci 5:1–10CrossRefGoogle Scholar
  25. Dukes JS, Mooney HA (1999) Does global change increase the success of plant invaders? Trends Ecol Evol 14:135–139CrossRefPubMedGoogle Scholar
  26. Faber P (2000) Grass wars: good intentions gone awry: Why would anyone bring an alien cordgrass into San Francisco Bay? Calif Coast Ocean 16:14–17Google Scholar
  27. Fortune PM, Schierenbeck K, Ayres D, Bortolus A, Catrice O, Brown S, Ainouche ML (2008) The enigmatic invasive Spartina densiflora: a history of hybridizations in a polyploidy context. Mol Ecol 17:4304–4316CrossRefPubMedGoogle Scholar
  28. Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70:303–307CrossRefGoogle Scholar
  29. Hester MW, Mendelssohn IA, McKee KL (2001) Species and population variation to salinity stress in Panicum, Spartina patens and Spartina alterniflora: morphological and physiological constraints. Environ Exp Bot 46:277–297CrossRefGoogle Scholar
  30. Howard R, Mendelssohn IA (1999) Salinity as a constraint on growth of oligohaline marsh macrophytes. I. Species variation in stress tolerance. Am J Bot 86:785–794CrossRefPubMedGoogle Scholar
  31. Kavi Kishor PB, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37:300–311CrossRefPubMedGoogle Scholar
  32. Kittelson PM, Boyd MJ (1997) Mechanism of expansion for an introduced species of cordgrass, Spartina densiflora, in Humboldt Bay, California. Estuaries 20:770–778CrossRefGoogle Scholar
  33. Leger EA, Rice KJ (2003) Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecol Lett 6:257–264CrossRefGoogle Scholar
  34. Loebl M, van Beusekom JEE, Reise K (2006) Is spread of the neophyte Spartina anglica recently enhanced by increasing temperatures? Aquat Ecol 40:315–324CrossRefGoogle Scholar
  35. Maron JL, Vila M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280CrossRefGoogle Scholar
  36. Marschner H (2012) Mineral nutrition of higher plants, 3rd edn. Academic Press, LondonGoogle Scholar
  37. Molina-Montenegro MA, Naya DE (2012) Latitudinal patterns in phenotypic plasticity and fitness-related traits: assessing the climatic variability hypothesis (CVH) with an invasive plant species. PLoS ONE 7(10):e47620. doi: 10.1371/journal.pone.004762 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Nieva FJ, Diaz-Espejo A, Castellanos EM, Figueroa ME (2001) Field variability of invading populations of Spartina densiflora Brong. grown in different habitats of the Odiel marshes (SW Spain). Estuar Coast Shelf Sci 52:515–527CrossRefGoogle Scholar
  39. Nieva FJ, Castellanos EM, Castillo JM, Figueroa ME (2005) Clonal growth and tiller demography of the invader cordgrass Spartina densiflora Brongn. at two contrasting habitats in SW European salt marshes. Wetlands 25:122–129CrossRefGoogle Scholar
  40. Olsson K, Ǻgren J (2002) Latitudinal population differentiation in phenology, life history and flower morphology in the perennial herb Lythrum salicaria. J Evol Biol 15:983–996CrossRefGoogle Scholar
  41. Pandit MK, White SM, Pocock MJO (2014) The contrasting effects of genome size, chromosome number and ploidy level on plant invasiveness: a global analysis. New Phytol 203:697–703CrossRefPubMedGoogle Scholar
  42. Parker VT, Callaway JC, Schile LM, Vasey MC, Herbert ER (2011) Climate change and San Francisco Bay-Delta tidal wetlands. San Franc Estuary Watershed Sci 9:1–15. Retrieved from: http://www.escholarship.org/uc/item/8j20685w
  43. Perazzolo M, Pinheiro F (1991) Aspectos anatómicos e adaptativos das partes vegetativas de Spartina densiflora Brong. (Gramineae) da marisma do estuário da lagoa dos Patos-RS. Acta Bot Bras 5:3–16CrossRefGoogle Scholar
  44. Richards CL (2012) Epigenetics: linking genotype and phenotype in development and evolution. Integr Comp Biol 52:547–549CrossRefGoogle Scholar
  45. Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993CrossRefPubMedGoogle Scholar
  46. Ruprecht E, Fenesi A, Nijs N (2014) Are plasticity in functional traits and constancy in performance traits linked with invasiveness? An experimental test comparing invasive and naturalized plant species. Biol Invasions 16:1359–1372CrossRefGoogle Scholar
  47. Scheiner SM (2001) MANOVA: multiple response variables and multi-species interactions. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments, 2nd edn. Oxford University Press, Oxford, pp 99–115Google Scholar
  48. Shumway SW, Bertness MD (1994) Patch size effects on marsh secondary succession mechanisms. Ecology 75:564–568CrossRefGoogle Scholar
  49. Song YB, Yu FH, Keser L et al (2013) United we stand, divided we fall: a meta-analysis of experiments on clonal integration and its relationship to invasiveness. Oecologia 171:317–327CrossRefPubMedGoogle Scholar
  50. Spicher D, Josselyn M (1985) Spartina (Gramineae) in northern California: distribution and taxonomic notes. Madroño 32:158–167Google Scholar
  51. Strong DR, Ayres DR (2013) Ecological and evolutionary misadventures of Spartina. Annu Rev Ecol Evol Syst 44:389–410CrossRefGoogle Scholar
  52. te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Kubesová M, Pysek P (2012) The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot Lond 109:19–45CrossRefGoogle Scholar
  53. Thompson JD (1991) The biology of an invasive plant. What makes Spartina anglica so successful? Bioscience 41:393–401CrossRefGoogle Scholar
  54. Valiela I, Teal JM (1974) Nutrient limitation of salt marsh vegetation. In: Reimold RJ, Queen WH (eds) Ecology of halophytes. Academic Press, New York, pp 547–563Google Scholar
  55. Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116CrossRefGoogle Scholar
  56. Vilà M, Corbin JD, Ducks JS, Pino J, Smith SD (2007) Linking plant invasions to global change. In: Canadell J, Pataki D, Pitelka L (eds) Terrestrial ecosystems in a changing world. Springer, New York, pp 93–102CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland (outside the USA) 2016

Authors and Affiliations

  • Brenda J. Grewell
    • 1
    Email author
  • Jesús M. Castillo
    • 2
  • Meghan J. Skaer Thomason
    • 1
  • Rebecca E. Drenovsky
    • 3
  1. 1.USDA-ARS Exotic and Invasive Weeds Research Unit, Department of Plant SciencesUniversity of CaliforniaDavisUSA
  2. 2.Departamento de Biología Vegetal y EcologíaUniversidad de SevillaApartadoSpain
  3. 3.Biology DepartmentJohn Carroll UniversityUniversity HeightsUSA

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