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Adaptive phenotypic plasticity and competitive ability deployed under a climate change scenario may promote the invasion of Poa annua in Antarctica

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Abstract

Antarctica is one of the less prone environments for plant invasions, nevertheless a growing number of non-native species have been registered in the last decades with negative effects on native flora. Here we assessed adaptive phenotypic plasticity in three photoprotective traits (non-photochemical quenching, total soluble sugars, and de-epoxidation state of xanthophylls cycle), and fitness-related traits (maximum quantum yield, photosynthetic rate and total biomass) in the invasive species Poa annua and Deschampsia antarctica under current conditions of water availability and those projected by climate change models. In addition, two manipulative experiments in controlled and field conditions were conducted to evaluate the competitive ability and survival of both species under current and climate change conditions. Moreover, we performed an experiment with different water availabilities to assess cell damage as a potential mechanism involved in the competitive ability deployed in both species. Finally, was assessed the plasticity and biomass of both species subject to factorial abiotic scenarios (water × temperature, and water × nutrients) ranging from current to climate change condition. Overall, results showed that P. annua had greater phenotypic plasticity in photoprotective strategies, higher performance, and greater competitive ability and survival than D. antarctica under current and climate change conditions. Also, cell damage, assessed by lipid peroxidation, was significantly greater in D. antarctica when grown in presence of P. annua compared when grown alone. Finally, P. annua showed a greater plasticity and biomass than D. antarctica under the factorial abiotic scenarios, being more evident under a climate change scenario (i.e., higher soil moisture). Our study suggests that the high adaptive plasticity and competitive ability deployed by P. annua under current and climate change conditions allows it to cope with harsh abiotic conditions and could help explain its successful invasion in the Antarctica.

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References

  • Alberdi M, Bravo LA, Gutiérrez A, Gidekel M, Corcuera LJ (2002) Ecophysiology of Antarctic vascular plants. Physiol Plant 115:479–486

    Article  CAS  PubMed  Google Scholar 

  • Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 147–169

    Google Scholar 

  • Bokhorst S, Huiskes A, Convey P, Sinclair BJ, Lebouvier M, Van de Vijver B, Wall DH (2011) Microclimate impacts of passive warming methods in Antarctica: implications for climate change studies. Polar Biol 34:1421–1435

    Article  Google Scholar 

  • Chown SL, Huiskes AHL, Gremmen NJM, Lee JE, Terauds A, Crosbie K et al (2012) Continent-wide risk assessment for the establishment of nonindigenous species in Antarctica. Proc Nat Acad Sci USA 109:4938–4943

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chwedorzewska KJ (2008) Poa annua L. in Antarctic: searching for the resource of introduction. Polar Biol 31:263–268

    Article  Google Scholar 

  • Chwedorzewska KJ (2009) Terrestrial Antarctic ecosystems in the changing world: an overview. Pol Polar Res 30:263–276

    Article  Google Scholar 

  • Chwedorzewska KJ, Gielwanowska I, Szczuka E, Bochenek A (2008) High anatomical and low genetic diversity in Deschampsia antarctica Desv. from King George Island, the Antarctic. Pol Polar Res 29:377–386

    Google Scholar 

  • Chwedorzewska KJ, Giełwanowska I, Olech M, Molina-Montenegro MA, Wódkiewicz M, Galera H (2015) Poa annua L. in the maritime Antarctic—an overview. Polar Rec 51:637–643

    Article  Google Scholar 

  • Convey P (2008) Non-native species in Antarctic terrestrial and freshwater environments: presence, sources, impacts and predictions. In: Rogan-Finnemore M (ed) Non-native species in the Antarctic, proceedings. Gateway Antarctica Special Publication, Christchurch, pp 97–130

    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 invisibility. J Ecol 88:528–534

    Article  Google Scholar 

  • Durand LZ, Goldstein G (2001) Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126:345–354

    Article  Google Scholar 

  • Egert M, Tevini M (2002) Influence of drought on some physiological parameters symptomatic for oxidative stress in leaves of chives (Allium schoenoprasum). Environ Exp Bot 48:43–49

    Article  CAS  Google Scholar 

  • Ellis-Evans JC, Walton D (1990) The process of colonization in Antarctic terrestrial and freshwater ecosystems. Polar Biol 3:151–163

    Google Scholar 

  • Flexas J, Ribas-Carbó M, Bota J, Galmés J, Henckle M, Martínez-Cañellas S et al (2006) Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. New Phytol 172:73–82

    Article  CAS  PubMed  Google Scholar 

  • Fox GA (1993) Failure time analysis: emergence, flowering, survivorship, and other waiting times. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University, Oxford, pp 253–289

    Google Scholar 

  • Fox AJ, Cooper PR (1998) Climate-change indicators from archival aerial photography of the Antarctic Peninsula. Ann Glaciol 27:636–642

    Google Scholar 

  • Frenot Y, Gloaguen JC, Trehen P (1997) Climate change in Kergulen Islands and colonization of recently deglaciated areas by Poa kergulensis and P. annua. In: Battaglia B (ed) Antarctic communities: species structure and survival. Cambridge University Press, Cambridge, pp 358–366

    Google Scholar 

  • Frenot Y, Aubry M, Misset MT, Gloaguen JC, Gourret JP, Lebouvier M (1999) Phenotypic plasticity and genetic diversity in Poa annua L. (Poaceae) at Crozet and Kerguelen Islands (subantarctic). Polar Biol 22:302–310

    Article  Google Scholar 

  • Frenot Y, Chown SL, Whinam J, Selkirk PM, Convey P, Skotnicki M et al (2005) Biological Invasions in the Antarctic: extent, impacts and implications. Biol Rev 80:45–72

    Article  PubMed  Google Scholar 

  • García-Plazaola JI, Matsubara S, Osmond CB (2007) The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Funct Plant Biol 34:759–773

    Article  Google Scholar 

  • Godoy O, Valladares F, Castro-Díez P (2011) Multispecies comparison reveals that invasive and native plants differ in their traits but not in their plasticity. Funct Ecol 25:1248–1253

    Article  Google Scholar 

  • Grace JB (1995) On the measurement of plant competition intensity. Ecology 76:305–308

    Article  Google Scholar 

  • Heres AM, Martínez-Vilalta J, Claramunt B (2012) Growth patterns in relation to drought-induced mortality at two Scots pine (Pinus sylvestris L.) sites in NE Iberian Peninsula. Trees 26:621–630

    Article  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hughes KA, Pertierra LR, Molina-Montenegro MA, Convey P (2015) Biological invasions in terrestrial Antarctica: what is the current status and can we respond? Biodivers Conserv 24:1031–1055

    Article  Google Scholar 

  • Huiskes AHL, Gremmen NJM, Bergstrom DM, Frenot Y, Hughes KA, Imura S et al (2014) Aliens in Antarctica: assessing transfer of plant propagules by human visitors to reduce invasion risk. Biol Conserv 171:278–284

    Article  Google Scholar 

  • Hulme PE (2008) Phenotypic plasticity and plant invasions: is it all Jack? Funct Ecol 22:3–7

    Article  Google Scholar 

  • Hutchinson GE (1957) Concluding remarks. Cold Spring Harb Symp Quant Biol 22:415–427

    Article  Google Scholar 

  • Intergovernmental Panel on Climate Change (IPCC) (2013) The physical science basis. www.ipcc.ch

  • Kennedy AD (1995) Antarctic terrestrial ecosystem response to global environmental change. Ann Rev Ecol Syst 26:683–704

    Article  Google Scholar 

  • Komárkowá V, Poncet S, Poncet J (1985) Two native Antarctic vascular plants, Deschampsia antarctica and Colobanthus quitensis: a new southernmost locality and other localities in the Antarctic Peninsula area. Arct Alp Res 17:401–416

    Article  Google Scholar 

  • Lambers H, Chapin FS, Pons TL (1998) Plant physiological ecology. Springer, Heidelberg

    Book  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 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • McDowell SCL (2002) Photosynthetic characteristics of invasive and non-invasive species of Rubus (Rosaceae). Am J Bot 89:1431–1438

    Article  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S et al (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–466

    Article  CAS  PubMed  Google Scholar 

  • Molina-Montenegro MA, Cavieres LA (2010) Variación altitudinal de los atributos morfo-fisiológicos en dos especies de plantas alto-andinas y sus implicancias contra la fotoinhibición. Gayana Bot 67:1–11

    Article  Google Scholar 

  • 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:e47620

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Molina-Montenegro MA, Cleland EE, Watts SM, Broitman BR (2012a) Can a breakdown in competition-colonization tradeoff help explain the success of exotic species in the California flora? Oikos 121:389–395

    Article  Google Scholar 

  • Molina-Montenegro MA, Torres-Díaz C, Carrasco-Urra F, González-Silvestre L, Gianoli E (2012b) Plasticidad fenotípica en dos poblaciones antárticas de Colobanthus quitensis (caryophyllaceae) bajo un escenario simulado de cambio global. Gayana Bot 69:152–160

    Article  Google Scholar 

  • Molina-Montenegro MA, Carrasco-Urra F, Rodrigo C, Convey P, Valladares F, Gianoli E (2012c) Occurrence of the non-native annual Bluegrass on the Antarctic mainland and its negative effects on the native plants. Conserv Biol 26:717–723

    Article  PubMed  Google Scholar 

  • Molina-Montenegro MA, Peñuelas J, Munné-Bosh S, Sardans J (2012d) Higher plasticity in ecophysiological traits enhances the performance and invasion success of Taraxacum officinale (dandelion) in alpine environments. Biol Invasions 14:21–33

    Article  Google Scholar 

  • Molina-Montenegro MA, Palma-Rojas C, Alcayaga-Olivares Y, Oses R, Corcuera LJ, Cavieres LA, Gianoli E (2013a) Ecophysiological plasticity and local differentiation help explain the invasion success of Taraxacum officinale (dandelion) in South America. Ecography 36:718–730

    Article  Google Scholar 

  • Molina-Montenegro MA, Ricote-Martínez N, Muñoz-Ramírez C, Torres-Díaz C, Gómez-González S, Gianoli E (2013b) Positive interactions between the lichen Usnea antarctica (Parmeliaceae) and the native flora in Maritime Antarctica. J Veg Sci 24:463–472

    Article  Google Scholar 

  • Molina-Montenegro MA, Carrasco-Urra F, Acuña-Rodríguez IS, Oses R, Torres-Díaz C, Chwedorzewska KJ (2014) Assessing the importance of human activities for the establishment of the invasive Poa annua in the Antarctica. Polar Res 33:21425

    Article  Google Scholar 

  • Moline MA, Claustre H, Frazer TK, Schofield O, Vernet M (2004) Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Glob Change Biol 10:1073–1980

    Article  Google Scholar 

  • Mozdzer TH, Megonigal JP (2012) Jack-and-Master trait responses to elevated CO2 and N: a comparison of native and introduced Phragmites australis. PLoS One 7:e42794

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Munné-Bosch S, Alegre L (2000) Changes in carotenoids, tocopherols and diterpenes during drought and recovery and biological significance of chlorophyll loss in Rosmarinus officinalis plants. Planta 210:925–931

    Article  PubMed  Google Scholar 

  • Muth NZ, Pigliucci M (2007) Implementation of a novel framework for assessing species plasticity in biological invasions: responses of Centaurea and Crepis to Phosphorus and water availability. J Ecol 95:1001–1013

    Article  Google Scholar 

  • Nobel PS (2005) Physicochemical and environmental plant physiology. Academic Press, New York

    Google Scholar 

  • Ogaya R, Peñuelas J, Asensio D, Llusià J (2011) Chlorophyll fluorescence responses to temperature and water availability in two co-dominant Mediterranean shrub and tree species in a long-term field experiment simulating climate change. Environ Exp Bot 73:89–93

    Article  CAS  Google Scholar 

  • Olech M, Chwedorzewska KJ (2011) The first appearance and establishment of alien vascular plant in natural habitats on the forefield of retreating glacier in Antarctica. Antarct Sci 23:153–154

    Article  Google Scholar 

  • Palacio-López K, Gianoli E (2011) Invasive plants do not display greater phenotypic plasticity than their native or non-invasive counterparts: a meta-analysis. Oikos 120:1393–1401

    Article  Google Scholar 

  • Pertierra LR, Lara F, Benayas F, Hughes KA (2013) Poa pratensis L., current status of the longest-established non-native vascular plant in the Antarctic. Polar Biol 36:1473–1481

    Article  Google Scholar 

  • Pichancourt JB, van Klinken RD (2012) Phenotypic plasticity influences the size, shape and dynamics of the geographic distribution of an invasive plant. PLoS One 7:e32323

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367

    Article  PubMed  Google Scholar 

  • Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882

    Article  CAS  PubMed  Google Scholar 

  • Pintó-Marijuan M, Munné-Bosch S (2013) Ecophysiology of invasive plants: osmotic adjustment and antioxidants. Trends Plant Sci 18:660–666

    Article  PubMed  Google Scholar 

  • Potvin C, Tardif S (1988) Sources of variability and experimental designs in growth chambers. Funct Ecol 2:122–130

    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, ecological studies. Springer, Berlin, pp 97–126

    Google Scholar 

  • Rejmánek M, Richardson DM, Higgins SI, Pitcairn MJ, Grotkopp E (2005) Ecology of invasive plants: state of the art. In: Mooney HA, Mack RN, McNeely JA, Neville LE, Schei PJ, Waage JK (eds) Invasive alien species a new synthesis. Island Press, Washington, pp 104–116

    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 

  • Robinson SA, Wasley J, Tobin AK (2003) Living on the edge—plants and global change in continental and maritime Antarctica. Glob Change Biol 9:1681–1717

    Article  Google Scholar 

  • Roe JH (1934) A colorimetric method for the determination of fructose in blood and urine. J Biol Chem 107:15–22

    CAS  Google Scholar 

  • Sexton JP, McKay JK, Sala A (2002) Plasticity and genetic diversity may allow saltcedar to invade cold climates in North America. Ecol Appl 12:1652–1660

    Article  Google Scholar 

  • Smith RIL (1996) Introduced plants in Antarctica: potential impacts and conservation issues. Biol Conserv 76:135–146

    Article  Google Scholar 

  • Smith RIL (2003) The enigma of Colobanthus quitensis and Deschampsia antarctica in Antarctica. In: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys Publishers, Leiden, pp 234–239

    Google Scholar 

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

    Article  Google Scholar 

  • Tian XR, Lei YB (2007) Physiological responses of wheat seedlings to drought and UV-B radiation. Effect of exogenous sodium nitroprusside application. Russ J Plant Physiol 54:676–682

    Article  CAS  Google Scholar 

  • Turner J, Colwell SR, Marshall GJ, Lachlan-Cope TA, Carleton AM, Jones PD et al (2005) Antarctic climate change during the last 50 years. Int J Climatol 25:279–294

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Vilà M, Weiner J (2004) Are invasive plant species better competitors than native plant species? Evidence from pair-wise experiments. Oikos 105:229–238

    Article  Google Scholar 

  • Wasley JS, Robinson A, Lovelock CE, Popp M (2006) Climate change manipulations show Antarctic flora is more strongly affected by elevated nutrients than water. Glob Change Biol 12:1800–1812

    Article  Google Scholar 

  • Wurzburger N, Ford-Miniat C (2014) Drought enhances symbiotic dinitrogen fixation and competitive ability of a temperate forest tree. Oecologia 174:1117–1126

    Article  PubMed  Google Scholar 

  • Zamora P, Rasmussen S, Pardo A, Prieto H, Zúñiga GE (2010) Antioxidant responses of in vitro shoots of Deschampsia antarctica to polyethylene glycol treatment. Antarct Sci 22:163–169

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River

    Google Scholar 

  • Zúñiga-Feest A, Bascuñán-Godoy L, Reyes-Diaz M, Bravo LA, Corcuera LJ (2009) Is survival after ice encasement related with sugar distribution in organs of the antarctic plants Deschampsia antarctica Desv. (Poaceae) and Colobanthus quitensis (Kunth) Bartl. (Caryophyllaceae)? Polar Biol 32:583–591

    Article  Google Scholar 

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Acknowledgments

We are grateful to Fernando Carrasco-Urra for their assistance in the field and logistic support from Antarctic station “Arctowski”. Also we acknowledge the financial and logistic support of the Chilean Antarctic Institute (INACH Project T-14-08 and G_22_11).

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Authors and Affiliations

  1. Instituto de Ciencias Biológicas, Universidad de Talca, Campus Talca, Avda. Lircay s/n, Talca, Chile

    Marco A. Molina-Montenegro & Carolina Galleguillos

  2. Facultad de Ciencias del Mar, Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Universidad Católica del Norte, Coquimbo, Chile

    Marco A. Molina-Montenegro, Rómulo Oses & Ian S. Acuña-Rodríguez

  3. Departamento Científico, Instituto Antártico Chileno (INACH), Punta Arenas, Chile

    Paris Lavín & Jorge Gallardo-Cerda

  4. Departamento de Ciencias Básicas, Facultad de Ciencias, Universidad del Bío-Bío, Chillán, Chile

    Cristian Torres-Díaz

  5. Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile

    Beatriz Diez

  6. Departamento de Ingeniería Hidráulica y Ambiental, Pontificia Universidad Católica de Chile, Santiago, Chile

    Gonzalo E. Pizarro

  7. Laboratorio de Anatomía y Ecología Funcional de Plantas, Facultad de Ciencias, Pontificia Universidad Católica de Valparaíso, Campus Curauma, Valparaiso, Chile

    Cristian Atala

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  1. Marco A. Molina-Montenegro
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  2. Carolina Galleguillos
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Molina-Montenegro, M.A., Galleguillos, C., Oses, R. et al. Adaptive phenotypic plasticity and competitive ability deployed under a climate change scenario may promote the invasion of Poa annua in Antarctica. Biol Invasions 18, 603–618 (2016). https://doi.org/10.1007/s10530-015-1033-x

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