Abstract
Phenotypic variation within species can have community- and ecosystem-level effects. Such variation may be particularly important in ecosystem engineers, including many invasive species, because of the strong influence of these species on their surrounding communities and environment. We combined field surveys and glasshouse experiments to investigate phenotypic variation within the invasive common reed, Phragmites australis, among four estuarine source sites along the east coast of North America. Field surveys revealed variation in P. australis height and stem density among source sites. In a glasshouse environment, percent germination of P. australis seeds also varied across source sites. To test the degree to which phenotypic variation in P. australis reflected genetic or environmental differences, we conducted a glasshouse common garden experiment assessing the performance of P. australis seedlings from the four source sites across a salinity gradient. Populations maintained differences in morphology and growth in a common glasshouse environment, indicating a genetic component to the observed phenotypic variation. Despite this variation, experimentally increased porewater salinity consistently reduced P. australis stem density, height, and biomass. Differences in these morphological metrics are important because they are correlated with the impacts of invasive P. australis on the ecological communities it invades. Our results indicate that both colonization and spread of invasive P. australis will be dependent on the environmental and genetic context. Additional research on intraspecific variation in invasive species, particularly ecosystem engineers, will improve assessments of invasion impacts and guide management decisions in estuarine ecosystems.
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References
Able, Kenneth, Stacy Hagan, and Steven Brown. 2003. Mechanisms of marsh habitat alteration due to Phragmites: response of young-of-the-year mummichog (Fundulus heteroclitus) to treatment for Phragmites. Estuaries 26: 484–494.
Achenbach, Luciana, and Hans Brix. 2013. Can differences in salinity tolerance explain the distribution of four genetically distinct lineages of Phragmites australis in the Mississippi River Delta? Hydrobiologia 737: 5–23.
Achenbach, Luciana, Franziska Eller, Loc Xuan Nguyen, and Hans Brix. 2013. Differences in salinity tolerance of genetically distinct Phragmites australis clones. AoB Plants 5: plt019. https://doi.org/10.1093/aobpla/plt019.
Amsberry, Lindsay, Michael A. Baker, Patrick J. Ewanchuk, and Mark D. Bertness. 2000. Clonal integration and the expansion of Phragmites australis. Ecological Applications 10: 1110–1118.
Barrett, Spencer C.H. 2000. Microevolutionary influences of global changes on plant invasions. In Invasive Species in a Changing World, ed. Harold A. Mooney and Richard J. Hobbs, 115–139. Washington, DC: Island Press.
Bastlová, Daša, Hana Čížková, Marek Bastl, and Jan Květ. 2004. Growth of Lythrum salicaria and Phragmites australis plants originating from a wide geographical area: response to nutrient and water supply. Global Ecology and Biogeography 13: 259–271.
Bolnick, Daniel I., Priyanga Amarasekare, Márcio S. Araújo, Reinhard Bürger, Jonathan M. Levine, Mark Novak, Volker H.W. Rudolf, Sebastian J. Schreiber, Mark C. Urban, and David A. Vasseur. 2011. Why intraspecific trait variation matters in ecology. Trends in Ecology and Evolution 26: 183–192.
Burdick, David M., and Raymond Konisky. 2003. Determinants of expansion for Phragmites australis, common reed, in natural and impacted coastal marshes. Estuaries 26: 407–416.
Burdick, David M., Robert Buchsbaum, and Eric Holt. 2001. Variation in soil salinity associated with expansion of Phragmites australis in salt marshes. Environmental and Experimental Botany 46: 247–261.
Chambers, Randolph M., Laura A. Meyerson, and Kristin Saltonstall. 1999. Expansion of Phragmites australis into tidal wetlands of North America. Aquatic Botany 64: 261–273.
Chauvaud, Laurent, Janet K. Thompson, James E. Cloern, and Gérard Thouzeau. 2003. Clams as CO2 generators: the Potamocorbula amurensis example in San Francisco Bay. Limnology and Oceanography 48: 2086–2092.
Clevering, Olga A., Hans Brix, and Jaroslava Lukavská. 2001. Geographic variation in growth responses in Phragmites australis. Aquatic Botany 69: 89–108.
Cronin, James T., Ganesh P. Bhattarai, Warwick J. Allen, and Laura A. Meyerson. 2015. Biogeography of a plant invasion: plant-herbivore interactions. Ecology 96: 1115–1127.
De Kroon, Hans, and Risto Kalliola. 1995. Shoot dynamics of the giant grass Gynerium sagittatum in Peruvian Amazon floodplains, a clonal plant that does show self-thinning. Oecologia 101: 124–131.
Fortune, P.M., K. Schierenbeck, D. Ayres, A. Bortolus, O. Catrice, S. Brown, and M.L. Ainouche. 2008. The enigmatic invasive Spartina densiflora: a history of hybridizations in a polyploidy context. Molecular Ecology 17: 4304–4316.
Friedman, Jannice, and Spencer C.H. Barrett. 2009. Wind of change, new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Annals of Botany 103: 1515–1527.
Gotelli, Nicholas J., and Aaron M. Ellison. 2013. A primer of ecological statistics. 2nd ed. Sunderland: Sinauer Associates Inc..
Greene, Valerie E., Lindsay J. Sullivan, Janet K. Thompson, and Wim J. Kimmerer. 2011. Grazing impacts of the invasive clam Corbula amurensis on the microplankton assemblage of the northern San Francisco Estuary. Marine Ecology Progress Series 431: 183–193.
Grewell, Brenda, Jesús Castillo, Meghan S. Thomason, and Rebecca Drenovsky. 2016. Phenotypic plasticity and population differentiation in response to salinity in the invasive cordgrass Spartina densiflora. Biological Invasions 18: 2175–2187.
Grosholz, Edwin D. 2001. Small spatial-scale differentiation among populations of an introduced colonial invertebrate. Oecologia 129: 58–64.
Grosholz, Edwin D. 2002. Ecological and evolutionary consequences of coastal invasions. Trends in Ecology and Evolution 17: 22–27.
Hara, T., J. van Der Toorn, and J.H. Mook. 1993. Growth dynamics and size structure of shoots of Phragmites australis, a clonal plant. Journal of Ecology 81: 47–60.
Hastings, Alan, Kim Cuddington, Kendi F. Davies, Christopher J. Dugaw, Sarah Elmendorf, Amy Freestone, Susan Harrison, Matthew Holland, John Lambrinos, Urmilla Malvadkar, Brett A. Melbourne, Kara Moore, Caz Taylor, and Diane Thomson. 2005. The spatial spread of invasions: new developments in theory and evidence. Ecology Letters 8: 91–101.
Hazelton, Eric L.G., Thomas J. Mozdzer, David M. Burdick, Karin M. Kettenring, and Dennis F. Whigham. 2014. Phragmites australis management in the United States: 40 years of methods and outcomes. AoB Plants 6: plu001. https://doi.org/10.1093/aobpla/plu001.
Howard, Rebecca J. 2010. Intraspecific Variation in growth of marsh macrophytes in response to salinity and soil type: implications for wetland restoration. Estuaries and Coasts 33: 127–138.
Hughes, A. Randall, Brian D. Inouye, Marc T.J. Johnson, Nora Underwood, and Mark Velland. 2008. Ecological consequences of genetic diversity. Ecology Letters 11: 609–623.
Hughes, A. Randall, Forest R. Schenck, Jeanne Bloomberg, Torrance C. Hanley, Dongmei Feng, Tarik C. Gouhier, R. Edward Beighley, and David L. Kimbro. 2016. Biogeographic gradients in ecosystem processes of the invasive ecosystem engineer Phragmites australis. Biological Invasions 18: 2577–2595.
Jackson, Donald A. 1993. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74: 2204–2214.
Katsanevakis, Stelios, Inger Wallentinus, Argyro Zenetos, Erkki Leppäkoski, Melih Ertan Çinar, Bayram Oztürk, Michal Grabowski, Daniel Golani, and Ana C. Cardoso. 2014. Impacts of invasive alien marine species on ecosystem services and biodiversity: a pan-European review. Aquatic Invasions 9: 391–423.
Keller, Barbara E.M. 2000. Plant diversity in Lythrum, Phragmites and Typha marhes, Massachusetts, USA. Wetlands Ecology and Management 8: 391–401.
Kettenring, Karin M., and Dennis F. Whigham. 2009. Seed viability and seed dormancy of non-native Phragmites australis in suburbanized and forested watersheds of the Chesapeake Bay, USA. Aquatic Botany 91: 199–204.
Kettenring, Karin M., Melissa K. McCormick, Heather M. Baron, and Dennis F. Whigham. 2010. Phragmites australis (common reed) invasion in the Rhode River subestuary of the Chesapeake Bay: disentangling the effects of foliar nutrients, genetic diversity, patch size, and seed viability. Estuaries and Coasts 33: 118–126.
Killgore, K. Jack, Raymond P. Morgan, and Nancy B. Rybicki. 1989. Distribution and abundance of fishes associated with submersed aquatic plants in the Potomac River. North American Journal of Fisheries Management 9: 101–111.
King, Ryan S., William V. DeLuca, Dennis F. Whigham, and Peter P. Marra. 2007. Threshold effects of coastal urbanization on Phragmites australis (common reed) abundance and foliar nitrogen in Chesapeake Bay. Estuaries and Coasts 30: 469–481.
Langeland, Kenneth A. 1996. Hydrilla verticillata (L. F.) Royle (Hydrocharitaceae), “The perfect aquatic weed”. Castanea 61: 293–304.
Lissner, Jørgen, and Hans-Henrik Schierup. 1997. Effects of salinity on the growth of Phragmites australis. Aquatic Botany 55: 247–260.
Marks, M., B. Lapin, and J. Randall. 1994. Phragmites australis (P. communis): threats, management and monitoring. Natural Areas Journal 14: 285–294.
Martin, Laura J., and Bernd Blossey. 2013. The runaway weed: costs and failures of Phragmites australis management in the USA. Estuaries and Coasts 36: 626–632.
Martincic, J., V. Guberac, and S. Maric. 1997. Influence of winter rye (Secale cereale L.) seed size on germ and rootlet length, and grain yield. Rost Vyroba 43: 95–100.
Mateos-Naranjo, Enrique, and Susana Redondo-Gómez. 2015. Interpopulation differences in salinity tolerance of the invasive cordgrass Spartina densiflora: implications for invasion process. Estuaries and Coasts 39: 98–107.
Mauchamp, André, and François Mésleard. 2001. Salt tolerance in Phragmites australis populations from coastal Mediterranean marshes. Aquatic Botany 70: 39–52.
McCormick, Melissa K., Karin M. Kettenring, Heather M. Baron, and Dennis F. Whigham. 2010. Extent and mechanisms of Phragmites australis spread in brackish wetlands in a subestuary of the Chesapeake Bay, Maryland (USA). Wetlands 30: 67–74.
McNaughton, S.J. 1966. Ecotype function in Typha community-type. Ecological Monographs 36: 297–325.
McNaughton, S.J. 1975. R- and K-selection in Typha. The American Naturalist 109: 251–261.
Meyerson, Laura A., Kristin Saltonstall, Lisamarie Windham, Erik Kiviat, and Stuart Findlay. 2000. A comparison of Phragmites australis in freshwater and brackish marsh environments in North America. Wetlands Ecology and Management 8: 89–103.
Minchinton, Todd E., Juliet C. Simpson, and Mark D. Bertness. 2006. Mechanisms of exclusion of native coastal marsh plants by an invasive grass. Journal of Ecology 94: 342–354.
Mozder, Thomas J., and Patrick J. Megonigal. 2012. Jack-and-master trait responses to elevated CO2 and N: a comparison of native and introduced Phragmites australis. PloS One 7: e42794.
Mozder, Thomas J., and Joseph C. Zieman. 2010. Ecophysiological differences between genetic lineages facilitate the invasion of non-native Phragmites australis in North American Atlantic coast wetlands. Journal of Ecology 98: 451–458.
Mozder, Thomas J., Joshua S. Caplan, Rachel N. Hager, C. Edward Proffitt, and Laura A. Meyerson. 2016. Contrasting trait responses to latitudinal climate variation in two lineages of an invasive grass. Biological Invasions 18: 2649–2660.
Neira, Carlos, Lisa A. Levin, and Edwin D. Grosholz. 2005. Benthic macrofaunal communities of three sites in San Francisco Bay invaded by hybrid Spartina, with comparison to uninvaded habitats. Marine Ecology Progress Series 292: 111–126.
Neira, Carlos, Edwin D. Grosholz, Lisa A. Levin, and Rachael Blake. 2006. Mechanisms generating modification of benthos following tidal flat invasion by a Spartina hybrid. Ecological Applications 16: 1391–1404.
Parker, I.M., D. Simberloff, W.M. Lonsdale, K. Goodell, M. Wonham, P.M. Karieva, M.H. Williamson, B. Von Holle, P.B. Moyle, J.E. Byers, and L. Goldwasser. 1999. Impact: toward a framework for understanding the ecological effects of invaders. Biological Invasions 1: 3–19.
R Core Team. 2016. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing http://www.R-project.org/.
R Studio Team. 2016. RStudio: integrated development for R. Boston: RStudio, Inc. http://www.rstudio.com/.
Ricciardi, Anthony, Martha F. Hoopes, Michael P. Marchetti, and Julie L. Lockwood. 2013. Progress toward understanding the ecological impacts of nonnative species. Ecological Monographs 83: 263–282.
Richards, Christina L., Oliver Bossdorf, Norris Z. Muth, Jessica Gurevitch, and Massimo Pigliucci. 2006. Jack of all trades, master of some? One the role of phenotypic plasticity in plant invasions. Ecology Letters 9: 981–993.
Ruiz, Gregory M., James T. Carlton, Edwin D. Grosholz, and Anson H. Hines. 1997. Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. American Zoologist 37: 621–632.
Ruiz, Gregory M., Paul W. Fofonoff, and Anson H. Hines. 1999. Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnology and Oceanography 44: 950–972.
Ruiz, Gregory M., Paul W. Fofonoff, James T. Carlton, Marjorie J. Wonham, and Anson H. Hines. 2000. Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annual Review of Ecology and Systematics 31: 481–531.
Saltonstall, Kirstin. 2003. A rapid method for identifying the origin of North American Phragmites populations using RFLP Analysis. Wetlands 23: 1043–1047.
Saltonstall, Kristin. 2002. Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proceedings of the National Academy of Sciences 99: 2445–2449.
Saltonstall, Kristin, and J. Court Stevenson. 2007. The effect of nutrients on seedling growth of native and introduced Phragmites australis. Aquatic Botany 86: 331–336.
Sax, Dov F., John J. Stachowicz, James H. Brown, John F. Bruno, Michael N. Dawson, Steven D. Gaines, Richard K. Grosberg, Alan Hastings, Robert D. Holt, Margaret M. Mayfield, Mary I. O’Connor, and William R. Rice. 2007. Ecological and evolutionary insights from species invasions. Trends in Ecology and Evolution 22: 465–471.
Serafy, Joseph E., Riginal M. Harrell, and Linda M. Hurley. 1994. Mechanical removal of Hydrilla on the Potomac River, Maryland: local impacts on vegetation and associated fishes. Journal of Freshwater Ecology 2: 135–143.
Spencer, David F., and Gregory G. Ksander. 2006. Estimating Arundo donax ramet recruitment using degree-day based equations. Aquatic Botany 85: 282–288.
Stockwell, Craig A., Andrew P. Hendry, and Michael T. Kinnison. 2003. Contemporary evolution meets conservation biology. Trends in Ecology and Evolution 18: 94–101.
Strayer, David L., Valerie T. Eviner, Jonathan M. Jeschke, and Michael L. Pace. 2006. Understanding the long-term effects of species invasions. Trends in Ecology and Evolution 21: 645–651.
Talley, Theresa S., and Lisa A. Levin. 2001. Modification of sediments and macrofauna by an invasive marsh plant. Biological Invasions 3: 51–68.
Tepolt, C.K. 2015. Adaptation in marine invasions: a genetic perspective. Biological Invasions 17: 887–903.
Vasquez, Edward A., Edward P. Glenn, J. Jed Brown, Glenn R. Guntenspergen, and Stephen G. Nelson. 2005. Salt tolerance underlies the cryptic invasion of North American salt marshes by an introduced haplotype of the common reed Phragmites australis (Poaceae). Marine Ecology Progress Series 298: 1–8.
Weber, Ewald, and Bernhard Schmid. 1998. Latitudinal population differentiation in two species of Solidago (Asteraceae) introduced into Europe. American Journal of Botany 85: 1110–1121.
Whitham, Thomas G., William P. Young, Gregory D. Martinsen, Catherine A. Gehring, Jennifer A. Schweitzer, Stephen M. Shuster, Gina M. Wimp, Dylan G. Fischer, Joseph K. Bailey, Richard L. Lindroth, Scott Woolbright, and Cheryl R. Kuske. 2003. Community and ecosystem genetics: a consequence of the extended phenotype. Ecology Ecological Society of America 84: 559–573.
Williams, Susan L., and Edwin D. Grosholz. 2008. The invasive species challenge in estuarine and coastal environments: marrying management and science. Estuaries and Coasts 3: 3–20.
Zedler, Joy B., and Suzanne Kercher. 2004. Causes and consequences of invasive plants in wetlands: opportunities, opportunists, and outcomes. Critical Review in Plant Science 23: 431–452.
Acknowledgements
Elise Grape, Jeanne Bloomberg, Adar Thau, Shannon Freyer, and Daniel Von Staats assisted in the field and lab. Dongmei Feng helped proofread the manuscript. Two anonymous reviewers provided valuable feedback on the manuscript. This project was funded by a Northeastern University Tier1 grant to E. Beighley, D. Kimbro, and R. Hughes. This is contribution 356 from the Northeastern University Marine Science Center.
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Fig. S1
Diagrams depicting (a) the experimental design and (b) salinity treatment methodology of the glasshouse salinity experiment (GIF 288 kb)
Fig. S2
Correlations among morphological measures of P. australis panicles. Panicle morphological measures are displayed along the main diagonal. For the morphological measures along the corresponding x- and y-axis, panels above the main diagonal display Pearson’s correlation coefficient (95% confidence intervals), and panels below the main diagonal display correlation scatterplots. Axes are displayed on the edge of the figure: length (cm), width (cm), square-root spikelet number, seed number per spikelet, and square-root weight (g) (GIF 46 kb)
Fig. S3
Scree plot for principal components analysis of Z-scale transformed panicle traits: length, width, spikelet number, seed number per spikelet, and weight. Observed eigenvalues are plotted as open bars and the expected distribution of eigenvalues generated by the broken-stick model are plotted as open circles (GIF 4 kb)
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Schenck, F.R., Hanley, T.C., Beighley, R.E. et al. Phenotypic Variation Among Invasive Phragmites australis Populations Does Not Influence Salinity Tolerance. Estuaries and Coasts 41, 896–907 (2018). https://doi.org/10.1007/s12237-017-0318-y
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DOI: https://doi.org/10.1007/s12237-017-0318-y