Skip to main content

Advertisement

Log in

Environmental Limits on the Spread of Invasive Phragmites australis into Upland Forests with Marine Transgression

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

A Correction to this article was published on 28 August 2021

This article has been updated

Abstract

Phragmites australis is a cosmopolitan grass that has transformed tidal wetlands in regions where it is invasive. The position of P. australis at the upland margin of tidal wetlands makes it likely to be among the earliest species to colonize uplands in marshes responding to sea-level rise; P. australis has been spreading in step with transgressive forest retreat. Considered a high light demanding species, the forest shade has been thought to keep this prolific species in check. In this study, we surveyed the distribution of P. australis across the marsh-forest ecotone, with particular attention to low-light areas in the forest understory, an environmental setting that has been largely overlooked in investigations of this well-studied species. We found P. australis to be present and well-established in forest canopy cover of up to 87.4%. However, canopy cover was significantly and negatively related to P. australis density in a multivariate model describing the species’ distribution in the ecotone. To test the species’ growth in shade conditions corresponding to the forest understory, we performed a greenhouse shading experiment. While photosynthetic parameters and growth rates were reduced in shade treatments, shade-grown individuals exhibited relatively high rates of photosynthesis in light-response tests, and there was no difference between the species’ performance in partial and deep shade treatments. We conclude that, while P. australis prefers high light conditions, it is able to colonize and survive low-light conditions in closed forest. By colonizing forest understory areas prior to other salt-tolerant species, P. australis is prepositioned to be the dominant species during saltwater intrusion and forest retreat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Change history

References  

  • Amsberry, L., M.A. Baker, P.J. Ewanchuk, and M.D. Bertness. 2000. Clonal integration and the expansion of Phragmites australis. Ecological Applications 10: 1110–1118.

    Article  Google Scholar 

  • An, S., X. Liu, B. Wen, X. Li, P. Qi, and K. Zhang. 2020. Comparison of the photosynthetic capacity of Phragmites australis in five habitats in saline-alkaline wetlands. Plants 9: 1317.

    Article  CAS  Google Scholar 

  • Anisfeld, S.C., K.R. Cooper, and A.C. Kemp. 2017. Upslope development of a tidal marsh as a function of upland land use. Global Change Biology 23: 755–766.

    Article  Google Scholar 

  • Arzandeh, S., and J. Wang. 2003. Monitoring the change of Phragmites distribution using satellite data. Canadian Journal of Remote Sensing 29: 24–35.

    Article  Google Scholar 

  • Bart, D., and J.M. Hartman. 2000. Environmental determinants of Phragmites australis expansion in a New Jersey salt marsh: An experimental approach. Oikos 89: 59–69.

    Article  Google Scholar 

  • Bart, D., and J.M. Hartman. 2002. Environmental constraints on early establishment of Phragmites australis in salt marshes. Wetlands 22: 201–213.

    Article  Google Scholar 

  • Bourgeau-Chavez, L.L., K.P. Kowalski, M.L. Carlson Mazur, K.A. Scarbrough, R.B. Powell, C.N. Brooks, B. Huberty, L.K. Jenkins, E.C. Banda, and D.M. Galbraith. 2013. Mapping invasive Phragmites australis in the coastal Great Lakes with ALOS PALSAR satellite imagery for decision support. Journal of Great Lakes Research 39: 65–77.

    Article  Google Scholar 

  • Burdick, D.M., R. Buchsbaum, and E. Holt. 2001. Variation in soil salinity associated with expansion of Phragmites australis in salt marshes. Environmental and Experimental Botany 46: 247–261.

    Article  CAS  Google Scholar 

  • Caplan, J.S., R.N. Hager, J.P. Megonigal, and T.J. Mozdzer. 2015. Global change accelerates carbon assimilation by a wetland ecosystem engineer. Environmental Research Letters 10: 115006.

  • Chambers, R.M., K.J. Havens, S. Killeen, and M. Berman. 2008. Common reed Phragmites australis occurrence and adjacent land use along estuarine shoreline in Chesapeake Bay. Wetlands 28: 1097–1103.

    Article  Google Scholar 

  • Chambers, R.M., L.A. Meyerson, and K. Saltonstall. 1999. Expansion of Phragmites australis into tidal wetlands of North America. Aquatic Botany 64: 261–273.

    Article  Google Scholar 

  • Correll, M.D., W. Hantson, T.P. Hodgman, B.B. Cline, C.S. Elphick, W.G. Shriver, E.L. Tymkiw, and B.J. Olsen. 2019. Fine-scale mapping of coastal plant communities in the Northeastern USA. Wetlands 39: 17–28.

    Article  Google Scholar 

  • Ekstam, B., R. Johannesson, and P. Milberg. 1999. The effect of light and number of diurnal temperature fluctuations on germination of Phragmites australis. Seed Science Research 9: 165–170.

    Article  Google Scholar 

  • Eller, F., H. Skálová, J.S. Caplan, G.P. Bhattarai, M.K. Burger, J.T. Cronin, W. Guo, X. Guo, E.L.G. Hazelton, and K.M. Kettenring. 2017. Cosmopolitan species as models for ecophysiological responses to global change: The common reed Phragmites australis. Frontiers in Plant Science 8: 1833.

    Article  Google Scholar 

  • Fagherazzi, S., S.C. Anisfeld, L.K. Blum, E.V. Long, R.A. Feagin, A. Fernandes, W.S. Kearney, and K. Williams. 2019. Sea level rise and the dynamics of the marsh-upland boundary. Frontiers in Environmental Science 7: 25.

    Article  Google Scholar 

  • Galinato, M.I., and A.G. Van der Valk. 1986. Seed germination traits of annuals and emergents recruited during drawdowns in the Delta Marsh, Manitoba, Canada. Aquatic Botany 26: 89–102.

    Article  Google Scholar 

  • Gedan, K.B., R. Epanchin-Niell, and M. Qi. 2020. Rapid land cover change in a submerging coastal county. Wetlands 40: 1717–1728.

    Article  Google Scholar 

  • Gedan, K.B., B.R. Silliman, and M.D. Bertness. 2009. Centuries of human-driven change in salt marsh ecosystems. Annual Review of Marine Science 1: 117–141.

    Article  Google Scholar 

  • Gedan, K.B., and E. Fernández-Pascual. 2019. Salt marsh migration into salinized agricultural fields: A novel assembly of plant communities. Journal of Vegetation Science 30: 1007–1016.

    Article  Google Scholar 

  • Gedan, K.B., M.L. Kirwan, E. Wolanski, E.B. Barbier, and B.R. Silliman. 2011. The present and future role of coastal wetland vegetation in protecting shorelines: Answering recent challenges to the paradigm. Climatic Change 106: 7–29.

    Article  Google Scholar 

  • Gucker, C. L. 2008. Phragmites australis. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory. Fire Effects Information System, [Online].

  • Guo, W., C. Lambertini, X. Li, L.A. Meyerson, and H. Brix. 2013. Invasion of Old World Phragmites australis in the New World: Precipitation and temperature patterns combined with human influences redesign the invasive niche. Global Change Biology 19: 3406–3422.

    Google Scholar 

  • Harrell, F.E., and M.C. Dupont. 2006. The Hmisc Package. R package version 3.0–12.

  • Haslam, S.M. 1973. Some aspects of the life history and autecology of Phragmites communis Trin: A review. Botany School: University of Cambridge, England.

    Google Scholar 

  • Heberling, J. Mason. 2014. Leaf-level photosynthesis. https://sites.google.com/site/fridleylab/home/protocols/Heberling_PhotosynthesisProtocol_Feb2014.pdf

  • Jobe, J.G.D. III, and K. Gedan. 2021. Species-specific responses of a marsh-forest ecotone plant community responding to climate change. Ecology 102:e03296.

  • Kettenring, K.M., M.K. McCormick, H.M. Baron, and D.F. Whigham. 2011. Mechanisms of Phragmites australis invasion: Feedbacks among genetic diversity, nutrients, and sexual reproduction. Journal of Applied Ecology 48: 1305–1313.

    Article  Google Scholar 

  • Kirwan, M.L., and K.B. Gedan. 2019. Sea-level driven land conversion and the formation of ghost forests. Nature Climate Change 9: 450–457.

    Article  Google Scholar 

  • Kirwan, M.L., and J.P. Megonigal. 2013. Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504: 53–60.

    Article  CAS  Google Scholar 

  • Kirwan, M.L., D.C. Walters, W.G. Reay, and J.A. Carr. 2016. Sea level driven marsh expansion in a coupled model of marsh erosion and migration. Geophysical Research Letters 43: 4366–4373.

    Article  Google Scholar 

  • Kiviat, E. 1987. Common reed (Phragmites australis). Exotic plants with identified detrimental impacts on wildlife habitats in New York. New York Chapter, The Wildlife Society, Annandale, NY: 22–30.

  • Kottler, E.J., and K. Gedan. 2020. Seeds of change: Characterizing the soil seed bank of a migrating salt marsh. Annals of Botany 125: 335–344.

    Article  Google Scholar 

  • Kuznetsova, A., P.B. Brockhoff, and R.H.B. Christensen. 2017. lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software 82: 1–26.

    Article  Google Scholar 

  • Laba, M., R. Downs, S. Smith, S. Welsh, C. Neider, S. White, M. Richmond, W. Philpot, and P. Baveye. 2008. Mapping invasive wetland plants in the Hudson River National Estuarine Research Reserve using QuickBird satellite imagery. Remote Sensing of Environment 112: 286–300.

    Article  Google Scholar 

  • Lessmann, J.M., H. Brix, V. Bauer, O.A. Clevering, and F. A. Comı́n. . 2001. Effect of climatic gradients on the photosynthetic responses of four Phragmites australis populations. Aquatic Botany 69: 109–126.

    Article  CAS  Google Scholar 

  • Li, F., Y. Li, H. Qin, and Y. Xie. 2011. Plant distribution can be reflected by the different growth and morphological responses to water level and shade in two emergent macrophyte seedlings in the Sanjiang Plain. Aquatic Ecology 45: 89–97.

    Article  CAS  Google Scholar 

  • Li, S., Z. Ge, L. Xie, W. Chen, L. Yuan, D. Wang, X. Li, and L. Zhang. 2018. Ecophysiological response of native and exotic salt marsh vegetation to waterlogging and salinity: Implications for the effects of sea-level rise. Scientific Reports 8: 1–13.

    Google Scholar 

  • Mamat, Z., U. Halik, P. Muhtar, I. Nurmamat, A. Abliz, and T. Aishan. 2016. Influence of soil moisture and electrical conductivity on the growth of Phragmites australis (Cav.) in the Keriya oasis, China. Environmental Earth Sciences 75: 423.

  • Marks, M., B. Lapin, and J. Randall. 1994. Phragmites australis (P. communis): Threats, management and monitoring. Natural Areas Journal 14: 285–294.

    Google Scholar 

  • Martin, L.J., and B. Blossey. 2013. The runaway weed: Costs and failures of Phragmites australis management in the USA. Estuaries and Coasts 36: 626–632.

    Article  Google Scholar 

  • McCormick, M.K., K.M. Kettenring, H.M. Baron, and D.F. Whigham. 2010. Extent and reproductive mechanisms of Phragmites australis spread in brackish wetlands in Chesapeake Bay, Maryland (USA). Wetlands 30: 67–74.

    Article  Google Scholar 

  • Meyerson, L.A., K. Saltonstall, R.M. Chambers, B.R. Silliman, M.D. Bertness, and D. Strong. 2009. Phragmites australis in eastern North America: a historical and ecological perspective. Salt marshes under global siege: 57–82.

  • Meyerson, L.A., K. Saltonstall, L. Windham, E. Kiviat, and S. Findlay. 2000. A comparison of Phragmites australis in freshwater and brackish marsh environments in North America. Wetlands Ecology and Management 8: 89–103.

    Article  CAS  Google Scholar 

  • Minchinton, T.E., J.C. Simpson, and M.D. Bertness. 2006. Mechanisms of exclusion of native coastal marsh plants by an invasive grass. Journal of Ecology 94: 342–354.

    Article  Google Scholar 

  • Mitchell, M., J. Herman, D.M. Bilkovic, and C. Hershner. 2017. Marsh persistence under sea-level rise is controlled by multiple, geologically variable stressors. Ecosystem Health and Sustainability 3: 1379888.

    Article  Google Scholar 

  • Pengra, B.W., C.A. Johnston, and T.R. Loveland. 2007. Mapping an invasive plant, Phragmites australis, in coastal wetlands using the EO-1 Hyperion hyperspectral sensor. Remote Sensing of Environment 108: 74–81.

    Article  Google Scholar 

  • Pezeshki, S.R., R.D. DeLaune, and W.H. Patrick Jr. 1990. Flooding and saltwater intrusion: Potential effects on survival and productivity of wetland forests along the US Gulf Coast. Forest Ecology and Management 33: 287–301.

    Article  Google Scholar 

  • Ripley, B., B. Venables, D.M. Bates, Hornik, K., A. Gebhardt, D. Firth, and M.B. Ripley. 2013. Package ‘mass.’

  • Rooth, J.E., J.C. Stevenson, and J.C. Cornwell. 2003. Increased sediment accretion rates following invasion by Phragmites australis: The role of litter. Estuaries 26: 475–483.

    Article  Google Scholar 

  • 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 99:2445-2449.

  • Saltonstall, K. and L.A. Meyerson. 2016. Phragmites australis: from genes to ecosystems. Biological Invasions 18:2415-2420.

  • Silliman, B.R., and M.D. Bertness. 2004. Shoreline development drives invasion of Phragmites australis and the loss of plant diversity on New England salt marshes. Conservation Biology 18: 1424–1434.

    Article  Google Scholar 

  • Smith, J.A.M. 2013. The role of Phragmites australis in mediating inland salt marsh migration in a Mid-Atlantic estuary. PloS One 8: e65091.

  • Tate, A.S., and L.L. Battaglia. 2013. Community disassembly and reassembly following experimental storm surge and wrack application. Journal of Vegetation Science 24: 46–57.

    Article  Google Scholar 

  • Tully, K., K. Gedan, R. Epanchin-Niell, A. Strong, E.S. Bernhardt, T. BenDor, M. Mitchell, J. Kominoski, T.E. Jordan, and S.C. Neubauer. 2019. The invisible flood: The chemistry, ecology, and social implications of coastal saltwater intrusion. BioScience 69: 368–378.

    Article  Google Scholar 

  • Wickham, H. 2016. ggplot2: Elegant Graphics for Data Analysis. Springer.

  • Wickham, H. 2017. tidyverse: easily install and load “Tidyverse” packages. R package version, 1(1).

  • Wickham, H., R. Francois, L. Henry, and K. Müller. 2015. dplyr: a grammar of data manipulation. R package version 0.4 3.

  • Windham, L., and J.G. Ehrenfeld. 2003. Net impact of a plant invasion on nitrogen-cycling processes within a brackish tidal marsh. Ecological Applications 13: 883–896.

    Article  Google Scholar 

  • Zedler, J.B., and S. Kercher. 2004. Causes and consequences of invasive plants in wetlands: opportunities, opportunists, and outcomes. critical Reviews in Plant sciences 23: 431–452.

Download references

Funding

This study was funded by award # F18AP00243 from the Mid-Atlantic Panel on Aquatic Invasive Species administered by Maryland Sea Grant. The statements, findings, conclusions, and recommendations are those of the authors and do not necessarily reflect the views of the Maryland Sea Grant. The study was also supported by a Harlan Undergraduate Research Scholarship from the Biological Sciences Department at George Washington University awarded to P. Shaw and NSF Graduate Research Fellowship award number 1746914 awarded to J. Jobe.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Keryn B. Gedan.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Communicated by Charles Simenstad

The original online version of this article was revised: Figure 3 was updated.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (PDF 584 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shaw, P., Jobe, J. & Gedan, K.B. Environmental Limits on the Spread of Invasive Phragmites australis into Upland Forests with Marine Transgression. Estuaries and Coasts 45, 539–550 (2022). https://doi.org/10.1007/s12237-021-00980-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-021-00980-9

Keywords

Navigation