Biological Invasions

, Volume 15, Issue 10, pp 2253–2264 | Cite as

Exotic species display greater germination plasticity and higher germination rates than native species across multiple cues

  • Claire E. WainwrightEmail author
  • Elsa E. Cleland
Original Paper


Rapid germination or flexible germination cues may be key traits that facilitate the invasion of exotic plant species in new environments. We investigated whether robustness or plasticity in response to environmental cues were more commonly exhibited by exotic than native species during germination, evidenced by (1) exhibiting consistently greater germination rate under a variety of conditions (robustness), or (2) increasing germination rate more strongly than native species in response to favorable conditions (plasticity). We conducted growth chamber germination trials of 12 native and 12 exotic species common to coastal sage scrub, a shrub-dominated Mediterranean-type ecosystem in California. Time to germination and percentage germination were recorded in response to variation in three environmental cues: temperature, day length, and soil moisture. Exotic species, especially annuals, displayed consistently higher germination percentages and more rapid germination than native species. Exotic germination percentages also responded more strongly when conditions were favorable (warm temperatures and high soil moisture), and germinated earlier than natives when conditions were indicative of typical growing season conditions in Mediterranean ecosystems (short day length and cool temperatures). Exotic species had more rapid and prolific germination across a variety of environmental cues and in response to increased resource availability compared with native species, indicating both germination plasticity and robustness. These traits may enable colonization of novel environments, particularly if they allow exotic species to establish earlier in the growing season than native species, setting the stage for seasonal priority effects.


Germination Invasion Phenology Plasticity Priority effects Robustness 



We wish to acknowledge the Kohn Lab and Roy Lab at the University of California, San Diego, for providing growth chamber space for this study. We also wish to thank the Kamprath Seed Company for their generous donation of seeds. This work was supported by a Mildred E. Mathias Graduate Student Research Grant from the University of California Natural Reserve System and an Educational Grant from the California Native Plant Society.

Supplementary material

10530_2013_449_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 15 kb)


  1. Abraham J, Corbin J, D’Antonio CM (2009) California native and exotic perennial grasses differ in their response to soil nitrogen, exotic annual grass density, and order of emergence. Plant Ecol 201:445–456CrossRefGoogle Scholar
  2. Baker HG (1974) The evolution of weeds. Annu Rev Ecol Syst 5:1–24CrossRefGoogle Scholar
  3. Bartolome JW (1979) Germination and seedling establishment in California annual grassland. J Ecol 67:273–281CrossRefGoogle Scholar
  4. Belyea LR, Lancaster J (1999) Assembly rules within a contingent ecology. Oikos 86:402–416CrossRefGoogle Scholar
  5. Black JN (1958) Competition between plants of different initial seed sizes in swards of subterranean clover (Trifolium subterraneum L.) with particular reference to leaf area and the light microclimate. Aust J Agric Res 9:299–318CrossRefGoogle Scholar
  6. Booth MS, Caldwell MM, Stark JM (2003) Overlapping resource use in three Great Basin species: implications for community invasibility and vegetation dynamics. J Ecol 91:36–48CrossRefGoogle Scholar
  7. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155CrossRefGoogle Scholar
  8. Brändle M, Stadler J, Klotz S, Brandl R (2003) Distributional range size of weedy plant species is correlated to germination patterns. Ecology 84:136–144CrossRefGoogle Scholar
  9. Burke MJW, Grime JP (1996) An experimental study of plant community invasibility. Ecology 77:776–790CrossRefGoogle Scholar
  10. Carlsen TM, Menke JW, Pavlik BM (2000) Reducing competitive suppression of a rare annual forb by restoring native California perennial grasslands. Restor Ecol 8:18–29CrossRefGoogle Scholar
  11. Chrobock T, Kempel A, Fischer M, van Kleunen M (2011) Introduction bias: cultivated alien plant species germinate faster and more abundantly than native species in Switzerland. Basic Appl Ecol 12:244–250CrossRefGoogle Scholar
  12. Cleland EE, Larios L, Suding KN (2012) Strengthening invasion filters to reassemble native plant communities: soil resources and phenological overlap. Restor Ecol Early View doi:  10.1111/j.1526-100X.2012.00896.x
  13. Coleman H, Levine J (2007) Mechanisms underlying the impacts of exotic annual grasses in a coastal California meadow. Biol Invasions 9:65–71CrossRefGoogle Scholar
  14. Cox RD, Allen EB (2008) Stability of exotic annual grasses following restoration efforts in southern California coastal sage scrub. J Appl Ecol 45:495–504CrossRefGoogle Scholar
  15. Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? a meta-analysis. Ecol Lett 14:419–431PubMedCrossRefGoogle Scholar
  16. Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534CrossRefGoogle Scholar
  17. Deering RH, Young TP (2006) Germination speeds of exotic annual and native perennial grasses in California and the potential benefits of seed priming for grassland restoration. Grasslands 16:14–15Google Scholar
  18. DeFalco L, Fernandez G, Nowak R (2007) Variation in the establishment of a non-native annual grass influences competitive interactions with Mojave Desert perennials. Biol Invasions 9:293–307CrossRefGoogle Scholar
  19. Donohue K, Pyle EH, Messiqua D, Heschel MS, Schmitt J (2001) Adaptive divergence in plasticity in natural populations of Impatiens capensis and its consequences for performance in novel habitats. Evolution 55:692–702PubMedCrossRefGoogle Scholar
  20. Droste T, Flory S, Clay K (2010) Variation for phenotypic plasticity among populations of an invasive exotic grass. Plant Ecol 207:297–306CrossRefGoogle Scholar
  21. Dyer AR, Fenech A, Rice KJ (2000) Accelerated seedling emergence in interspecific competitive neighbourhoods. Ecol Lett 3:523–529CrossRefGoogle Scholar
  22. Espigares T, Peco B (1993) Mediterranean pasture dynamics: the role of germination. J Veg Sci 4:189–194CrossRefGoogle Scholar
  23. Facelli M, Chesson P, Barnes N (2005) Differences in seed biology of annual plants in arid lands: a key ingredient of the storage effect. Ecology 86:2998–3006CrossRefGoogle Scholar
  24. Funk JL (2008) Differences in plasticity between invasive and native plants from a low resource environment. J Ecol 96:1162–1173CrossRefGoogle Scholar
  25. Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081PubMedCrossRefGoogle Scholar
  26. Funk JL, Cleland EE, Suding KN, Zavaleta ES (2008) Restoration through reassembly: plant traits and invasion resistance. Trends Ecol Evol 23:695–703PubMedCrossRefGoogle Scholar
  27. Godoy O, Richardson DM, Valladares F, Castro-Díez P (2009) Flowering phenology of invasive alien plant species compared with native species in three Mediterranean-type ecosystems. Ann Bot 103:485–494PubMedCrossRefGoogle Scholar
  28. Grime JP, Jeffrey DW (1965) Seedling establishment in vertical gradients of sunlight. J Ecol 53:621–642CrossRefGoogle Scholar
  29. Grime JP, Mason G, Curtis AV, Rodman J, Band SR (1981) A comparative study of germination characteristics in a local flora. J Ecol 69:1017–1059CrossRefGoogle Scholar
  30. Grman E, Suding KN (2010) Within-year soil legacies contribute to strong priority effects of exotics on native California grassland communities. Restor Ecol 18:664–670CrossRefGoogle Scholar
  31. Grotkopp E, Rejmánek M (2007) High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. Am J Bot 94:526–532PubMedCrossRefGoogle Scholar
  32. Gulmon SL (1992) Patterns of seed germination in Californian serpentine grassland species. Oecologia 89:27–31CrossRefGoogle Scholar
  33. Hamilton JG, Holzapfel C, Mahall BE (1999) Coexistence and interference between a native perennial grass and non-native annual grasses in California. Oecologia 121:518–526CrossRefGoogle Scholar
  34. Hickman JC (ed) (1993) The Jepson manual: higher plants of California. University of California Press, BerkeleyGoogle Scholar
  35. Hierro JL, Eren Ö, Khetsuriani L, Diaconu A, Török K, Montesinos D, Andonian K, Kikodze D, Janoian L, Villarreal D et al (2009) Germination responses of an invasive species in native and non-native ranges. Oikos 118:529–538Google Scholar
  36. Hoffmann AA, Parsons PA (1991) Evolutionary genetics and environmental stress. Oxford University Press, OxfordGoogle Scholar
  37. Kalisz S (1986) Variable selection on the timing of germination in Collinsia verna (Scrophulariaceae). Evolution 40:479–491CrossRefGoogle Scholar
  38. Leishman MR, Thomson VP (2005) Experimental evidence for the effects of additional water, nutrients and physical disturbance on invasive plants in low fertility Hawkesbury Sandstone soils, Sydney, Australia. J Ecol 93:38–49CrossRefGoogle Scholar
  39. Levine JM, Rees M (2004) Effects of temporal variability on rare plant persistence in annual systems. Am Nat 164:350–363PubMedCrossRefGoogle Scholar
  40. Levine JM, McEachern AK, Cowan C (2008) Rainfall effects on rare annual plants. J Ecol 96:795–806CrossRefGoogle Scholar
  41. Lieth H (ed) (1974) Phenology and seasonality modeling. Springer, BerlinGoogle Scholar
  42. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  43. Marushia RG, Cadotte MW, Holt JS (2010) Phenology as a basis for management of exotic annual plants in desert invasions. J Appl Ecol 47:1290–1299CrossRefGoogle Scholar
  44. Peñuelas J, Filella I, Zhang X, Llorens L, Ogaya R, Lloret F, Comas P, Estiarte M, Terradas J (2004) Complex spatiotemporal phenological shifts as a response to rainfall changes. New Phytol 161:837–846CrossRefGoogle Scholar
  45. Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  46. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  47. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2009) nlme: Linear and nonlinear mixed effects models. R Package version 3.1-103.
  48. Poorter H, Lambers H (1986) Growth and competitive ability of a highly plastic and a marginally plastic genotype of Plantago major in a fluctuating environment. Physiol Plant 67:217–222CrossRefGoogle Scholar
  49. Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: Where do we stand? In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 97–125Google Scholar
  50. R Development Core Team (2010) R: a language and environment for statistical computing.
  51. Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214CrossRefGoogle Scholar
  52. Rees M, Long M (1992) Germination biology and the ecology of annual plants. Am Nat 139:484–508CrossRefGoogle Scholar
  53. Rejmanek M (2000) Invasive plants: approaches and predictions. Austral Ecol 25:497–506CrossRefGoogle Scholar
  54. Reynolds SA, Corbin JD, D’Antonio CM (2001) The effects of litter and temperature on the germination of native and exotic grasses in a coastal California grassland. Madrono 48:230–235Google Scholar
  55. 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 9:981–993PubMedCrossRefGoogle Scholar
  56. Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693CrossRefGoogle Scholar
  57. Seabloom EW, Harpole WS, Reichman OJ, Tilman D (2003) Invasion, competitive dominance, and resource use by exotic and native California grassland species. PNAS 100:13384–13389PubMedCrossRefGoogle Scholar
  58. Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. J Ecol 82:328–343Google Scholar
  59. Sultan SE (2003) Phenotypic plasticity in plants: a case study in ecological development. Evol Dev 5:25–33PubMedCrossRefGoogle Scholar
  60. van Kleunen M, Johnson SD (2007) South African Iridaceae with rapid and profuse seedling emergence are more likely to become naturalized in other regions. J Ecol 95:674–681CrossRefGoogle Scholar
  61. van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245PubMedCrossRefGoogle Scholar
  62. Venable DL (2007) Bet hedging in a guild of desert annuals. Ecology 88:1086–1090PubMedCrossRefGoogle Scholar
  63. Verdú M, Traveset A (2005) Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86:1385–1394CrossRefGoogle Scholar
  64. Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478Google Scholar
  65. Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565CrossRefGoogle Scholar
  66. Wainwright CE, Wolkovich EM, Cleland EE (2012) Seasonal priority effects: implications for invasion and restoration in a semi-arid system. J Appl Ecol 49:234–241CrossRefGoogle Scholar
  67. Went FW (1949) Ecology of desert plants. II. The effect of rain and temperature on germination and growth. Ecology 30:1–13CrossRefGoogle Scholar
  68. Westoby M, Jurado E, Leishman M (1992) Comparative evolutionary ecology of seed size. Trends Ecol Evol 7:368–372PubMedCrossRefGoogle Scholar
  69. Williams DG, Mack RN, Black RA (1995) Ecophysiology of introduced Pennisetum setaceum on Hawaii: the role of phenotypic plasticity. Ecology 76:1569–1580CrossRefGoogle Scholar
  70. Wolkovich EM, Cleland EE (2011) The phenology of plant invasions: a community ecology perpective. Front Ecol Environ 9:287–294CrossRefGoogle Scholar
  71. Young TP, Chase JM, Huddleston RT (2001) Community succession and assembly. Ecol Restor 19:5–18Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Division of Biological Sciences, Ecology, Behavior and Evolution SectionUniversity of CaliforniaLa Jolla, San DiegoUSA

Personalised recommendations