, Volume 35, Issue 5, pp 877–888 | Cite as

Stand Age is Associated with Clonal Diversity, but Not Vigor, Community Structure, or Insect Herbivory in Chesapeake Bay Phragmites australis

  • Eric L. G. Hazelton
  • Melissa K. McCormick
  • Matthew Sievers
  • Karin M. Kettenring
  • Dennis F. Whigham
Original Research


Invasions are dynamic as both the invading organism and the invaded ecosystem change. Intrinsic changes to the invader (invasion process) can involve population level genetic and reproductive changes. Extrinsic changes (invasion effect) occur to the environment that is invaded (e.g., alterations to the physical environment), to the invaded plant community (e.g., changes in species diversity and composition or evolutionary changes), or to insect herbivory. To investigate how invasions change through time, we investigated both the process and effect of a Phragmites australis invasion by comparing young and old P. australis stands within two Chesapeake Bay subestuaries. We quantified clonal richness of P. australis stands, vigor of the invader, herbivore damage, and plant community composition. Our results indicate that only the population-scale genetics (clonal richness, genetic distance) changed over the course of 40 years. Clonal richness was lower in the old P. australis stands, likely due to intraspecific competition and/or initial colonization by fewer genotypes. The mean genetic distance among clones within old stands was lower than within young stands, suggesting that clones within old stands were mostly closely-related, while young stands were likely established by seeds from nearby stands and so were more representative of the local area. Clones in different old stands were genetically more distant from each other than those in young stands were from clones in other young stands. This pattern suggested that old stands were established by independent colonization events, while young patches were established by a mixture of seeds from local stands, which generated the lower average genetic distance between clones across young stands. We found that community composition, plant vigor, and herbivore damage to stems were similar across different age stands, which indicated that the effect of P. australis invasion becomes stable within a few decades. Over longer periods, the intrinsic invasion process may be more dynamic than the invasion effect.


Allee effects Clonal diversity Clonal plants Invasive plant Microsatellite markers Phragmites australis 



The authors are grateful to Louise McKenzie and Matthew Van Scoyoc for critical statistical advice, and Susan Cook-Patton for thoughtful comments on this manuscript. The manuscript greatly benefitted from comments by the editor and external reviewers. Jay O’Neill, Liza McFarland, and Rachel Dutko assisted in the lab and field. All microsatellite analyses were carried out at the Smithsonian Laboratory of Analytical Biology. This research was funded by NOAA (grant #NA09NOS4780214). A Smithsonian Institution Predoctoral Fellowship, Utah State University Ecology Center Student Research Support, Society of Wetland Scientists, and Delta Waterfowl provided additional support for EH.


  1. Ahee JC, Sinclair BJ, Dorkena ME (2013) A new species of Stenodiplosis (Diptera: Cecidomyiidae) on florets of the invasive common reed (Phragmites australis) and its effects on seed production. Canadian Entomologist 145(3):235–246CrossRefGoogle Scholar
  2. Allee WC (1931) Animal aggregations, a study in general sociology. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  3. Ally D, Ritland K, Otto SP (2010) Aging in a long-lived clonal tree. PLoS Biology 8:8CrossRefGoogle Scholar
  4. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Primer-e, Plymouth, p 214Google Scholar
  5. Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA (2007) Standardizing methods to address clonality in population studies. Molecular Ecology 16:5115–5139CrossRefPubMedGoogle Scholar
  6. Bart D, Burdick D, Chambers R, Hartman JM (2006) Human facilitation of Phragmites australis invasions in tidal marshes: a review and synthesis. Wetl Ecol Manag 14(1):53–65Google Scholar
  7. Bertness MD, Ewanchuk PJ, Silliman BR (2002) Anthropogenic modification of New England salt marsh landscapes. Proceedings of the National Academy of Sciences of the United States of America 99(3):1395–1398PubMedCentralCrossRefPubMedGoogle Scholar
  8. Blossey B, Schwarzlander M, Hafliger P, Casagrande R, Tewksbury L (2002) Common reed. In: Van Driesche R, Blossey B, Hoddle M, Lyon S, Reardon R (eds) Biological control of invasive plants in the Eastern United States. Forest Health Technology Enterprise Team, MorgantownGoogle Scholar
  9. Bruvo R, Michiels NK, D’Souza TG, Schulenburg H (2004) A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Molecular Ecology 13:2101–2106CrossRefPubMedGoogle Scholar
  10. Bullock JM, Clarke RT (2000) Long distance seed dispersal by wind: measuring and modelling the tail of the curve. Oecologia 124(4):506–521CrossRefGoogle Scholar
  11. Burdick DM, Konisky YA (2003) Determinants of expansion for Phragmites australis, common reed, in natural and impacted coastal marshes. Estuaries and Coasts 26(2):407–416CrossRefGoogle Scholar
  12. Cappuccino N (2004) Allee effect in an invasive alien plant, pale swallow‐wortVincetoxicum rossicum (Asclepiadaceae). Oikos 106(1):3–8CrossRefGoogle Scholar
  13. Chambers RM, Meyerson L, Saltonstall K (1999) Expansion of Phragmites australis into tidalwetlands of North America. Aquatic Botany 64(3–4):261–273CrossRefGoogle Scholar
  14. Chambers RM, Havens KJ, Killeen S, Berman M (2008) Common reed Phragmites australis occurrence and adjacent land use along estuarine shoreline in Chesapeake Bay. Wetlands 28:1097–1103CrossRefGoogle Scholar
  15. Clark LV, Jasieniuk M (2011) POLYSAT: an R package for polyploid microsatellite analysis. Molecular Ecology Resources 11(3):562–566CrossRefPubMedGoogle Scholar
  16. Corbin JD, D’Antonio CM (2012) Gone but not forgotten? Invasive plants’ legacies on community and ecosystem properties. Invasive Plant Science and Management 5(1):117–124CrossRefGoogle Scholar
  17. Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313(5789):966–968CrossRefPubMedGoogle Scholar
  18. Čurn V, Kubátová B, Vávřová P, Křiváčková-Suchá O, Čížková H (2007) Phenotypic and genotypic variation of Phragmites australis: comparison of populations in two human-made lakes of different age and history. Aquatic Botany 86(4):321–330CrossRefGoogle Scholar
  19. Davis HG, Taylor CM, Lambrinos JG, Strong DR (2004) Pollen limitation causes an Allee effect in a wind-pollinated invasive grass (Spartina alterniflora). Proceedings of the National Academy of Sciences of the United States of America 101(38):13804–13807PubMedCentralCrossRefPubMedGoogle Scholar
  20. Dennis B (2002) Allee effects in stochastic populations. Oikos 96(3):389–401CrossRefGoogle Scholar
  21. DeWoody JA, Schupp J, Kenefic L, Busch J, Murfitt L, Keim P (2004) Universal method for producing ROX-labeled size standards suitable for automated genotyping. Biology Techniques 37(3):348–352Google Scholar
  22. Douhovnikoff V, Mcbride JR, Dodd RS (2005) Salix exigua clonal growth and population dynamics in relation to disturbance regime variation. Ecology 86(2):446–452CrossRefGoogle Scholar
  23. Drake JM (2004) Allee effects and the risk of biological invasion. Risk Analysis 24(4):795–802CrossRefPubMedGoogle Scholar
  24. Ellstrand NC, Roose ML (1987) Patterns of genotypic diversity in clonal plant species. Am J Bot 74(1):123–131Google Scholar
  25. Eriksson O (1989) Seedling dynamics and life histories in clonal plants. Oikos 55:231–238CrossRefGoogle Scholar
  26. Eriksson O, Fröborg H (1996) “Windows of opportunity” for recruitment in long-lived clonal plants: experimental studies of seedling establishment in Vaccinium shrubs. Canadian Journal of Botany 74(9):1369–1374CrossRefGoogle Scholar
  27. Estrella S, Kneitel JM (2011) Invasion age and invader removal alter species cover and composition at the Suisun Tidal Marsh, California, USA. Diversity and Distributions 3(2):235–251CrossRefGoogle Scholar
  28. Farnsworth EJ, Meyerson LA (1999) Species composition and inter-annual dynamics of a freshwater tidal plant community following removal of the invasive grass, Phragmites australis. Biological Invasions 1:115–127CrossRefGoogle Scholar
  29. Findlay S, Groffman P, Dye S (2003) Effects of Phragmites australis removal on marsh nutrient cycling. Wetlands Ecology and Management 11:157–165CrossRefGoogle Scholar
  30. Hacker SD, Dethier MN (2012) Differing consequences of removing ecosystem-modifying invaders: significance of impact and community context to restoration potential. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, BerlinGoogle Scholar
  31. Ishii J, Kadono Y (2002) Factors influencing seed production of Phragmites australis. Aquatic Botany 72(2):129–141CrossRefGoogle Scholar
  32. Kettenring KM, Mock KE (2012) Genetic diversity, reproductive mode, and dispersal differ between the cryptic invader, Phragmites australis, and its native conspecific. Biological Invasions 14:2489–2504CrossRefGoogle Scholar
  33. Kettenring KM, Whigham DF (2009) Seed viability and seed dormancy of non-native Phragmites australis in suburbanized and forested watersheds of the Chesapeake Bay, USA. Aquatic Botany 91:199–204CrossRefGoogle Scholar
  34. Kettenring KM, McCormick MK, Baron HM, Whigham DF (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(1):118–126CrossRefGoogle Scholar
  35. Kettenring KM, McCormick MK, Baron HM, Whigham DF (2011) Mechanisms of Phragmites australis invasion: feedbacks among genetic diversity, nutrients, and sexual reproduction. Journal of Applied Ecology 48(5):1305–1313CrossRefGoogle Scholar
  36. King RS, DeLuca WV, Whigham DF, Marra PP (2007) Threshold effects of coastal urbanization on Phragmites australis (common reed) abundance and foliar nitrogen in ChesapeakeBay. Estuaries and Coasts 30:469–481CrossRefGoogle Scholar
  37. Koppitz H, Kuhl H (2000) To the importance of genetic diversity of Phragmites australis in the development of reed stands. Wetlands Ecology and Management 8:403–414CrossRefGoogle Scholar
  38. Koppitz H, Kuhl H, Hesse K, Kohl J-G (1997) Some aspects of the importance of genetic diversity in Phragmites australis (Cav.) Trin. Ex Steudel for the development of reed stands. Botanica Acta 110:217–223CrossRefGoogle Scholar
  39. Křiváčková-Suchá O, Vávřová P, Čížková H, Čurn V, Kubátová B (2007) Phenotypic and genotypic variation of Phragmites australis: a comparative study of clones originating from two populations of different age. Aquatic Botany 86(4):361–368CrossRefGoogle Scholar
  40. Lambert A, Casagrande R (2007) Characteristics of a successful estuarine invader: evidence of self-compatibility in native and non-native lineages of Phragmites australis. Marine Ecology Progress Series 337:299–301CrossRefGoogle Scholar
  41. Lambert AM, Winiarski K, Casagrande RA (2007) Distribution and impact of exotic gall flies (Lipara spp.) on native and exotic Phragmites australis. Aquatic Botany 86:163–170CrossRefGoogle Scholar
  42. Lambertini C, Gustafsson MH, Frydenberg J, Speranza M, Brix H (2008) Genetic diversity patterns in Phragmites australis at the population, regional and continental scales. Aquatic Botany 88(2):160–170CrossRefGoogle Scholar
  43. Lavoie C, Jean M, Delisle F, Létourneau G (2003) Exotic plant species of the St Lawrence River wetlands: a spatial and historical analysis. Journal of Biogeography 30(4):537–549CrossRefGoogle Scholar
  44. Legendre P, Legendre L (2012) Numerical ecology (vol. 20). Elsevier, AmsterdamGoogle Scholar
  45. McCormick J, Somes HA (1982) The coastal wetlands of Maryland. Jack McCormick and Associates, AnnapolisGoogle Scholar
  46. McCormick MK, Kettenring KM, Baron HM, Whigham DF (2010a) Spread of invasive Phragmites australis in estuaries with differing degrees of development: genetic patterns, Allee effects and interpretation. Journal of Ecology 98(6):1369–1378CrossRefGoogle Scholar
  47. McCormick MK, Kettenring KM, Baron HM, Whigham DF (2010b) Extent and reproductive mechanisms of Phragmites australis spread in brackish wetlands in Chesapeake Bay, Maryland (USA). Wetlands 30:67–74CrossRefGoogle Scholar
  48. Minchinton TE, Simpson JC, Bertness MD (2006) Mechanisms of exclusion of native coastal marsh plants by an invasive grass. Journal of Ecology 94(2):342–354CrossRefGoogle Scholar
  49. Mitchell ME, Lishawa SC, Geddes P, Larkin DJ, Treering D, Tuchman NC (2011) Time-dependent impacts of cattail invasion in a Great Lakes coastal wetland complex. Wetlands 31(6):1143–1149CrossRefGoogle Scholar
  50. Niering WA, Warren RS, Weymouth CG (1977) Our dynamic tidal marshes: vegetation changes as revealed by peat analysis. The Connecticut Arboretum Bulletin (22)Google Scholar
  51. Obbard DJ, Harris SA, Pannell JR (2006) Simple allelic-phenotype diversity and differentiation statistics for allopolyploids. Heredity 97(4):296–303CrossRefPubMedGoogle Scholar
  52. Orson RA, Warren RS, Niering WA (1987) Development of a tidal marsh in a New England river valley. Estuaries and Coasts 10(1):20–27CrossRefGoogle Scholar
  53. Pollux BJA, Jong MDE, Steegh A, Verbruggen E, van Groenendael JM, Ouborg NJ (2007) Reproductive strategy, clonal structure and genetic diversity in populations of the aquatic macrophyte Sparganium emersum in river systems. Molecular Ecology 16:313–325CrossRefPubMedGoogle Scholar
  54. Raicu P, Staicu S, Stoian V, Roman T (1972) The Phragmites communis Trin.chromosome complement in the Danube delta. Hydrobiologia 39:249–252CrossRefGoogle Scholar
  55. Rees GN, Baldwin DS, Watson GO, Perryman S, Nielson DL (2004) Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Antonie van Leeuwenhoek 86:339–347Google Scholar
  56. Rice D, Rooth JE, Stevenson JC (2000) Colonization and expansion of Phragmites australis in upper Chesapeake Bay tidal marshes. Wetlands 20:280–299CrossRefGoogle Scholar
  57. Rooth JE, Stevenson JC, Cornwell JC (2003) Increased sediment accretion rates following invasion by Phragmites australis: the role of litter. Estuaries and Coasts 26(2):475–483CrossRefGoogle Scholar
  58. Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proceedings of the National Academy of Sciences of the United States of America 99:2445–2449PubMedCentralCrossRefPubMedGoogle Scholar
  59. Saltonstall K (2003) Microsatellite variation within and among North American lineages of Phragmites australis. Molecular Ecology 12:1689–1702CrossRefPubMedGoogle Scholar
  60. Silvertown J (2008) The evolutionary maintenance of sexual reproduction: evidence from the ecological distribution of asexual reproduction in clonal plants. International Journal of Plant Sciences 169(1):157–168CrossRefGoogle Scholar
  61. Smithsonian Institution (1974) Investigations on Classification Categories for Wetlands of Chesapeake Bay Using Remotely Sensed Data. Annual Report. October 10, 1972 to October 9, 1973. Chesapeake Bay Center for Environmental Studies, Smithsonian Institution. Edgewater, MDGoogle Scholar
  62. Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends in Ecology and Evolution 21(11):645–651CrossRefPubMedGoogle Scholar
  63. Suding KN, Gross KL, Houseman GR (2004) Alternative states and positive feedbacks in restoration ecology. Trends in Ecology and Evolution 19(1):46–53CrossRefPubMedGoogle Scholar
  64. Taylor CM, Hastings A (2004) Allee effects in biological invasions. Ecology Letters 8(8):895–908CrossRefGoogle Scholar
  65. Taylor CM, Davis HG, Civille JC, Grevstad FS, Hastings A (2004) Consequences of an Allee effect in the invasion of a Pacific estuary by Spartina alterniflora. Ecology 85:3254–3266CrossRefGoogle Scholar
  66. Tewksbury L, Casagrande R, Blossey B, Hafliger P, Schwarzlander M (2002) Potential for biological control of Phragmites australis in North America. Biological Control 23(2):191–212CrossRefGoogle Scholar
  67. Tscharntke T (1999) Insects on common reed Phragmites australis: community structure and the impact of herbivory on shoot growth. Aquatic Botany 64(3):399–410CrossRefGoogle Scholar
  68. Tucker N (1938) A preliminary report on the salt marsh vegetation of Long Island, New York. New York State Museum, New YorkGoogle Scholar
  69. Utsumi S, Ando Y, Craig TP, Ohgushi T (2011) Plant genotypic diversity increases population size of a herbivorous insect. Philosophical Transactions of the Royal Society B 278(1721):3108–3115Google Scholar
  70. Vitousek PM (1990) Biological invasions and ecosystem processes: towards an integration of population biology and ecosystem studies. Oikos S57:7–13CrossRefGoogle Scholar
  71. Windham L, Meyerson LA (2003) Effects of common reed (Phragmites australis) expansions on nitrogen dynamics of tidal marshes of the northeastern US. Estuaries and Coasts 26(2):452–464CrossRefGoogle Scholar

Copyright information

© Society of Wetland Scientists 2015

Authors and Affiliations

  • Eric L. G. Hazelton
    • 1
    • 2
  • Melissa K. McCormick
    • 1
  • Matthew Sievers
    • 1
  • Karin M. Kettenring
    • 1
    • 2
  • Dennis F. Whigham
    • 1
  1. 1.Smithsonian Environmental Research CenterEdgewaterUSA
  2. 2.Ecology Center and Department of Watershed SciencesUtah State UniversityLoganUSA

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