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

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Abstract

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.

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References

  • 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 201:445–456

    Article  Google Scholar 

  • Baker HG (1974) The evolution of weeds. Annu Rev Ecol Syst 5:1–24

    Article  Google Scholar 

  • Bartolome JW (1979) Germination and seedling establishment in California annual grassland. J Ecol 67:273–281

    Article  Google Scholar 

  • Belyea LR, Lancaster J (1999) Assembly rules within a contingent ecology. Oikos 86:402–416

    Article  Google Scholar 

  • 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 9:299–318

    Article  Google Scholar 

  • Booth MS, Caldwell MM, Stark JM (2003) Overlapping resource use in three Great Basin species: implications for community invasibility and vegetation dynamics. J Ecol 91:36–48

    Article  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155

    Article  Google Scholar 

  • Brändle M, Stadler J, Klotz S, Brandl R (2003) Distributional range size of weedy plant species is correlated to germination patterns. Ecology 84:136–144

    Article  Google Scholar 

  • Burke MJW, Grime JP (1996) An experimental study of plant community invasibility. Ecology 77:776–790

    Article  Google Scholar 

  • Carlsen TM, Menke JW, Pavlik BM (2000) Reducing competitive suppression of a rare annual forb by restoring native California perennial grasslands. Restor Ecol 8:18–29

    Article  Google Scholar 

  • 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 12:244–250

    Article  Google Scholar 

  • 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

  • Coleman H, Levine J (2007) Mechanisms underlying the impacts of exotic annual grasses in a coastal California meadow. Biol Invasions 9:65–71

    Article  Google Scholar 

  • Cox RD, Allen EB (2008) Stability of exotic annual grasses following restoration efforts in southern California coastal sage scrub. J Appl Ecol 45:495–504

    Article  Google Scholar 

  • 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 14:419–431

    Article  PubMed  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534

    Article  Google Scholar 

  • 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 16:14–15

    Google Scholar 

  • 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 9:293–307

    Article  Google Scholar 

  • 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 55:692–702

    Article  PubMed  CAS  Google Scholar 

  • Droste T, Flory S, Clay K (2010) Variation for phenotypic plasticity among populations of an invasive exotic grass. Plant Ecol 207:297–306

    Article  Google Scholar 

  • Dyer AR, Fenech A, Rice KJ (2000) Accelerated seedling emergence in interspecific competitive neighbourhoods. Ecol Lett 3:523–529

    Article  Google Scholar 

  • Espigares T, Peco B (1993) Mediterranean pasture dynamics: the role of germination. J Veg Sci 4:189–194

    Article  Google Scholar 

  • 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 86:2998–3006

    Article  Google Scholar 

  • Funk JL (2008) Differences in plasticity between invasive and native plants from a low resource environment. J Ecol 96:1162–1173

    Article  Google Scholar 

  • Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079–1081

    Article  PubMed  CAS  Google Scholar 

  • Funk JL, Cleland EE, Suding KN, Zavaleta ES (2008) Restoration through reassembly: plant traits and invasion resistance. Trends Ecol Evol 23:695–703

    Article  PubMed  Google Scholar 

  • 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 103:485–494

    Article  PubMed  Google Scholar 

  • Grime JP, Jeffrey DW (1965) Seedling establishment in vertical gradients of sunlight. J Ecol 53:621–642

    Article  Google Scholar 

  • Grime JP, Mason G, Curtis AV, Rodman J, Band SR (1981) A comparative study of germination characteristics in a local flora. J Ecol 69:1017–1059

    Article  Google Scholar 

  • Grman E, Suding KN (2010) Within-year soil legacies contribute to strong priority effects of exotics on native California grassland communities. Restor Ecol 18:664–670

    Article  Google Scholar 

  • 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 94:526–532

    Article  PubMed  Google Scholar 

  • Gulmon SL (1992) Patterns of seed germination in Californian serpentine grassland species. Oecologia 89:27–31

    Article  Google Scholar 

  • Hamilton JG, Holzapfel C, Mahall BE (1999) Coexistence and interference between a native perennial grass and non-native annual grasses in California. Oecologia 121:518–526

    Article  Google Scholar 

  • Hickman JC (ed) (1993) The Jepson manual: higher plants of California. University of California Press, Berkeley

    Google Scholar 

  • 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 118:529–538

    Google Scholar 

  • Hoffmann AA, Parsons PA (1991) Evolutionary genetics and environmental stress. Oxford University Press, Oxford

    Google Scholar 

  • Kalisz S (1986) Variable selection on the timing of germination in Collinsia verna (Scrophulariaceae). Evolution 40:479–491

    Article  Google Scholar 

  • 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 93:38–49

    Article  Google Scholar 

  • Levine JM, Rees M (2004) Effects of temporal variability on rare plant persistence in annual systems. Am Nat 164:350–363

    Article  PubMed  Google Scholar 

  • Levine JM, McEachern AK, Cowan C (2008) Rainfall effects on rare annual plants. J Ecol 96:795–806

    Article  Google Scholar 

  • Lieth H (ed) (1974) Phenology and seasonality modeling. Springer, Berlin

    Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Marushia RG, Cadotte MW, Holt JS (2010) Phenology as a basis for management of exotic annual plants in desert invasions. J Appl Ecol 47:1290–1299

    Article  Google Scholar 

  • 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 161:837–846

    Article  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • 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. http://cran.r-project.org/web/packages/nlme/index.html

  • 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 67:217–222

    Article  Google Scholar 

  • 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 97–125

    Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. http://www.R-project.org

  • Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214

    Article  Google Scholar 

  • Rees M, Long M (1992) Germination biology and the ecology of annual plants. Am Nat 139:484–508

    Article  Google Scholar 

  • Rejmanek M (2000) Invasive plants: approaches and predictions. Austral Ecol 25:497–506

    Article  Google Scholar 

  • 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 48:230–235

    Google Scholar 

  • 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 9:981–993

    Article  PubMed  Google Scholar 

  • Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693

    Article  Google Scholar 

  • Seabloom EW, Harpole WS, Reichman OJ, Tilman D (2003) Invasion, competitive dominance, and resource use by exotic and native California grassland species. PNAS 100:13384–13389

    Article  PubMed  CAS  Google Scholar 

  • Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. J Ecol 82:328–343

    Google Scholar 

  • Sultan SE (2003) Phenotypic plasticity in plants: a case study in ecological development. Evol Dev 5:25–33

    Article  PubMed  Google Scholar 

  • 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 95:674–681

    Article  Google Scholar 

  • van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245

    Article  PubMed  Google Scholar 

  • Venable DL (2007) Bet hedging in a guild of desert annuals. Ecology 88:1086–1090

    Article  PubMed  Google Scholar 

  • Verdú M, Traveset A (2005) Early emergence enhances plant fitness: a phylogenetically controlled meta-analysis. Ecology 86:1385–1394

    Article  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565

    Article  Google Scholar 

  • Wainwright CE, Wolkovich EM, Cleland EE (2012) Seasonal priority effects: implications for invasion and restoration in a semi-arid system. J Appl Ecol 49:234–241

    Article  Google Scholar 

  • Went FW (1949) Ecology of desert plants. II. The effect of rain and temperature on germination and growth. Ecology 30:1–13

    Article  Google Scholar 

  • Westoby M, Jurado E, Leishman M (1992) Comparative evolutionary ecology of seed size. Trends Ecol Evol 7:368–372

    Article  PubMed  CAS  Google Scholar 

  • Williams DG, Mack RN, Black RA (1995) Ecophysiology of introduced Pennisetum setaceum on Hawaii: the role of phenotypic plasticity. Ecology 76:1569–1580

    Article  Google Scholar 

  • Wolkovich EM, Cleland EE (2011) The phenology of plant invasions: a community ecology perpective. Front Ecol Environ 9:287–294

    Article  Google Scholar 

  • Young TP, Chase JM, Huddleston RT (2001) Community succession and assembly. Ecol Restor 19:5–18

    Google Scholar 

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Acknowledgments

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.

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Correspondence to Claire E. Wainwright.

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Wainwright, C.E., Cleland, E.E. Exotic species display greater germination plasticity and higher germination rates than native species across multiple cues. Biol Invasions 15, 2253–2264 (2013). https://doi.org/10.1007/s10530-013-0449-4

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