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Effective suppression of established invasive Phragmites australis leads to secondary invasion in a coastal marsh

Published online by Cambridge University Press:  22 January 2021

Courtney D. Robichaud
Affiliation:
Ph.D Candidate, University of Waterloo, Waterloo, ON, Canada
Rebecca C. Rooney*
Affiliation:
Associate Professor, University of Waterloo, Waterloo, ON, Canada
*
Author for correspondence: Rebecca Rooney, University of Waterloo, 200 University Avenue West, Waterloo, ONTN2L 3G1, Canada. (Email: rrooney@uwaterloo.ca)

Abstract

Invasive species negatively impact vegetation communities. Invasive European common reed [Phragmites australis (Cav.) Trin. ex Steud. ssp. australis] is rapidly spreading throughout North American wetlands. As such, the suppression of P. australis populations is a goal of many managers, as its removal should provide an opportunity to restore native vegetation communities. In Ontario, managers applied a glyphosate-based herbicide to more than 400 ha of P. australis in ecologically significant coastal marshes, representing the first time this tool was used over standing water to suppress an invasive species in Canada. Using a before–after–control–impact monitoring design, we evaluated the efficacy of glyphosate-based herbicide at removing P. australis along a water-depth gradient and assessed the recovery of the vegetation community for 2 yr after treatment in relation to reference conditions. We found that herbicide suppressed more than 99% of P. australis 1 yr after treatment and worked effectively along the entire water-depth gradient (10 to 48 cm). However, the post-treatment vegetation community remains distinctive from reference marsh 2 yr after treatment. In many plots where P. australis was removed, nonnative European frog-bit (Hydrocharis morsus-ranae L.) is now dominant, likely aided by high lake-water levels.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Weed Science Society of America

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Footnotes

Associate Editor: Ryan M. Wersal, Minnesota State University

References

Ailstock, MS, Norman, CM, Bushmann, PJ (2001) Common reed Phragmites australis: control and effects upon biodiversity in freshwater nontidal wetlands. Restor Ecol 9:4959 CrossRefGoogle Scholar
Albert, A, Brisson, J, Belzile, F, Turgeon, J, Lavoie, C (2015) Strategies for a successful plant invasion: the reproduction of Phragmites australis in north-eastern North America. J Ecol 103:15291537 CrossRefGoogle Scholar
Baldwin, AH, Kettenring, KM, Whigham, DF (2010) Seed banks of Phragmites australis-dominated brackish wetlands: relationships to seed viability, inundation, and land cover. Aquatic Bot 93:163169 CrossRefGoogle Scholar
Ball, H, Jalava, J, King, T, Maynard, L, Potter, B, Pulfer, T (2003) The Ontario Great Lakes Coastal Weltand Atlas: A Summary of Information (1983–1997). Environment Canada. https://longpointbiosphere.com/download/Environment/Ontario. Great_.Lakes_.Coastal. Wetland.Atlas-2003.pdf. Accessed: May 3, 2020Google Scholar
Battaglin, WA, Meyer, MT, Kuivila, KM, Dietze, JE (2014) Glyphosate and its degradation product AMPA occur frequently and widely in U.S. soils, surface water, groundwater and precipitation. J Am Water Resour Assoc 50:275290 CrossRefGoogle Scholar
Beecraft, L, Rooney, RC (2020) Bioconcentration of glyphosate in wetland biofilms. Sci Tot Environ 756:143993 CrossRefGoogle ScholarPubMed
Bickerton, H (2015) Extent of European Common Reed (Phragmites australis ssp. australis) as a Threat to Species at Risk in Ontario. Ottawa, ON: Ontario Ministry of Natural Resources and Forestry, Natural Heritage Section. 22 pGoogle Scholar
Blossey, B (1999) Before, during and after: the need for long-term monitoring in invasive plant species management. Biol Invasions 1:301311 CrossRefGoogle Scholar
Bonello, JE, Judd, KE (2020) Plant community recovery after herbicide management to remove Phragmites australis in Great Lakes coastal wetlands. Restor Ecol 28:215221 CrossRefGoogle Scholar
Byun, C, de Blois, S, Brisson, J (2018) Management of invasive plants through ecological resistance. Biol Invasions 20:1327 CrossRefGoogle Scholar
Carlson, ML, Kowalski, KP, Wilcox, DA (2009) Promoting species establishment in a Phragmites-dominated Great Lakes Coastal wetland. Nat Areas J 29:263280 CrossRefGoogle Scholar
Carson, BD, Lishawa, SC, Tuchman, NC, Monks, AM, Lawrence, BA, Alberta, DA (2018) Harvesting invasive plants to reduce nutrient loads and produce bioenergy: an assessment of Great Lakes coastal wetlands. Ecosphere 9, 10.1002/ecs2.2320 CrossRefGoogle Scholar
Catling, PM, Mitrow, G (2011) The recent spread and potential distribution of Phragmites australis subsp. australis in Canada. Can Field-Nat 125:95104 CrossRefGoogle Scholar
Catling, PM, Mitrow, G, Haber, E, Posluszny, U, Charlton, WA (2003) The biology of Canadian weeds. 124. Hydrocharis morsus-ranae L. Can J Plant Science 7:57 Google Scholar
Catling, PM, Spicer, K, Lefkovitch, L (1988) Effects of the floating Hydrocharis morsus-ranae (Hydrocharitaceae) on some North American aquatic macrophytes. Nat Can 115:131137 Google Scholar
D’Antonio, CM, Meyerson, LA (2002) Exotic plant species as problems and solutions in ecological restoration. Restor Ecol 10:703713 CrossRefGoogle Scholar
de Mendiburu, F (2020) agricolae: Statistical Procedures for Agricultural Research. https://cran.r-project.org/web/packages/agricolae/index.html. Accessed: May 2, 2020Google Scholar
[DFO] Department of Fisheries and Oceans Canada (2019) Historical Monthly Mean Water Levels from the Coordinated Network for Each of the Great Lakes. http://www.tides.gc.ca/C&A/network_means-eng.html. Accessed: May 2, 2020Google Scholar
Derr, JF (2008) Common reed (Phragmites australis) response to mowing and herbicide application. Invasive Plant Sci Manag 1:1216 CrossRefGoogle Scholar
England, D (2019) Seeding Treatments to Enhance Seedling Performance of the Bulrushes Bolboschoenus maritiums, Schoenoplectus acutus, and S. americanus in Wetland Restorations. M.Sc thesis. Logan: Utah State University. https://digitalcommons.usu.edu/etd/7659 Google Scholar
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 . Biol Invasions 1:115127 CrossRefGoogle Scholar
Fox, J, Weisberg, S (2019) car: An {R} Companion to Applied Regression. 3rd ed. Thousand Oaks, CA: Sage. 608 p Google Scholar
Galatowitsch, S (2018) Plant community reassembly in restored wetlands. Pages 20032008 in Finlayson, CM, Everard, M, Irvine, K, McInnes, RJ, Middleton, BA, van Dam, AA, Davidson, NC, eds. The Wetland Book. Dordrecht: Springer CrossRefGoogle Scholar
Gioria, M, Jarošík, V, Pyšek, P (2014) Impact of invasions by alien plants on soil seed bank communities: emerging patterns. Perspect Plant Ecol Evol Syst 16:132142.CrossRefGoogle Scholar
González, E, Sher, AA, Anderson, RM, Bay, RF, Bean, DW, Bissonnete, GJ, Cooper, DJ, Dohrenwend, K, Eichhorst, KD, El Waer, H, Kennard, DK, Harms-Weissinger, R, Henry, AL, Makarick, LJ, Ostoja, SM, et al. (2017) Secondary invasions of noxious weeds associated with control of invasive Tamarix are frequent, idiosyncratic and persistent. Biol Conserv 213:106114 CrossRefGoogle Scholar
Gornish, E, Lennox, MS, Lewis, D, Tate, KW, Jackson, RD (2017) Comparing herbaceous plant communities in active and passive riparian restoration. PLoS ONE 12:112 CrossRefGoogle ScholarPubMed
Hazelton, ELG, Downard, R, Kettenring, KM, McCormick, MK, Whigham, DF (2018) Spatial and temporal variation in brackish wetland seedbanks: implications for wetland restoration following Phragmites control. Estuaries Coasts 41:6884 CrossRefGoogle Scholar
Hazelton, ELG, Mozdzer, TJ, Burdick, DM, Kettenring, KM, Whigham, DF (2014) Phragmites australis management in the United States: 40 years of methods and outcomes. AoB Plants 6:119 CrossRefGoogle ScholarPubMed
Health Canada (2020) Imazapyr, Habitat Aqua Proposed Registration Decision PRD2020-17. Health Canada, Pest Management Regulatory Authority. https://www.canada.ca/en/health-canada/services/consumer-product-safety/pesticides-pest-management/public/consultations/proposed-registration-decisions/2020/imazapyr-habitat-aqua/document.html. Accessed: January 11, 2021Google Scholar
Hess, MCM, Mesléard, F, Buisson, E (2019) Priority effects: emerging principles for invasive plant species management. Ecol Eng 127:4857 CrossRefGoogle Scholar
Hirtreiter, JN, Potts, DL (2012) Canopy structure, photosynthetic capacity and nitrogen distribution in adjacent mixed and monospecific stands of Phragmites australis and Typha latifolia . Plant Ecol 213:821829 CrossRefGoogle Scholar
Holdredge, C, Bertness, MD (2011) Litter legacy increases the competitive advantage of invasive Phragmites australis in New England wetlands. Biol Invasions 13:423433 CrossRefGoogle Scholar
Houlahan, JE, Findlay, CS (2004) Effect of invasive plant species on temperate wetland plant diversity. Conserv Biol 18:11321138 CrossRefGoogle Scholar
Howell, GMB (2017) Best Management Practices for Invasive Phragmites control. M.Sc thesis. Waterloo, ON, Canada: University of Waterloo. 105 pGoogle Scholar
Hunt, VM, Fant, JB, Steger, L, Hartzog, PE, Lonsdorf, EV, Jacobi, SK, Larkin, DJ (2017) PhragNet: crowdsourcing to investigate ecology and management of invasive Phragmites australis (common reed) in North America. Wetl Ecol Manag 25:607618 CrossRefGoogle Scholar
Judd, KE, Francoeur, SN (2019) Short-term impacts of Phragmites management on nutrient budgets and plant communities in Great Lakes coastal freshwater marshes. Wetl Ecol Manag 27:5574 CrossRefGoogle Scholar
Keddy, PA, Campbell, D (2019) The Twin Limit Marsh model: a non-equilibrium approach to predicting marsh vegetation on shorelines and in floodplains. Wetlands 40:667680 CrossRefGoogle Scholar
Keddy, PA, Reznicek, AA (1986) Great Lakes vegetation dynamics: the role of fluctuating water levels and buried seeds. J Great Lakes Res 12:2536 CrossRefGoogle Scholar
Kettenring, KM, Adams, CR (2011) Lessons learned from invasive plant control experiments: a systematic review and meta-analysis. J Appl Ecol 48:970979 CrossRefGoogle Scholar
Laughlin, DC (2014) Applying trait-based models to achieve functional targets for theory-driven ecological restoration. Ecol Lett 17:771784 CrossRefGoogle ScholarPubMed
Lei, C, Yuckin, SJ, Rooney, RC (2019) Rooting depth and below ground biomass in a freshwater coastal marsh invaded by European reed (Phragmites australis) compared with remnant uninvaded sites at Long Point, Ontario. Can Field Nat 133:364371 CrossRefGoogle Scholar
Lombard, KB, Tomassi, D, Ebersole, J (2012) Long-term management of an invasive plant: lessons from seven years of Phragmites australis control. Northeast Nat 19:181193 CrossRefGoogle Scholar
MacDougall, AS, Gilbert, B, Levine, JM (2009) Plant invasions and the niche. J Ecol 97:609615 CrossRefGoogle Scholar
Martin, LJ, Blossey, B (2013) The runaway weed: costs and failures of Phragmites australis management in the USA. Estuaries and Coasts 36:626632 CrossRefGoogle Scholar
Matthews, JW, Spyreas, G (2010) Convergence and divergence in plant community trajectories as a framework for monitoring wetland restoration progress. J Appl Ecol 47:11281136 CrossRefGoogle Scholar
McCormick, MK, Brooks, HEA, Whigham, DF (2016) Microsatellite analysis to estimate realized dispersal distance in Phragmites australis. Biol Invasions 18:24972504 CrossRefGoogle Scholar
McCune, B, Mefford, M.J (2015) PC-ORD. Multivariate Analysis of Ecological Data. Version 7.01. Gleneden Beach, OR: MjM SoftwareGoogle Scholar
Meyer, SW, Badzinski, SS, Petrie, SA, Ankney, CD (2010) Seasonal abundance and species richness of birds in common reed habitats in Lake Erie. J Wildl Manage 74:15591567 CrossRefGoogle Scholar
Meyerson, LA, Vogt, KA, Chambers, RM (2000) Linking the success of Phragmites to the alteration of ecosystem nutrient cycles. Pages 827844 in Weinstein, MP, Kreeger, DA, eds. Concepts and Controversies in Tidal Marsh Ecology. Dordrecht: Springer Google Scholar
Mohamed, MN, Wellen, C, Parsons, CT, Taylor, WD, Arhonditsis, G, Chomicki, KM, Boyd, D, Weidman, P, Mundle, SOC, Van Cappellen, P, Sharpley, AN, Haffner, DG (2019) Understanding and managing the re-eutrophication of Lake Erie: knowledge gaps and research priorities. Freshw Sci 38:675691 CrossRefGoogle Scholar
Monks, AM, Lishawa, SC, Wellons, KC, Albert, DA, Mudrzynski, B, Wilcox, DA (2019) European frogbit (Hydrocharis morsus-ranae) invasion facilitated by non-native cattails (Typha) in the Laurentian Great Lakes. J Great Lakes Res 45:912920 CrossRefGoogle Scholar
Moore, GE, Burdick, DM, Peter, CR, Keirstead, DR (2012) Belowground biomass of Phragmites australis in coastal marshes. Northeast Nat 19:611626 CrossRefGoogle Scholar
Myers, JP, Antoniou, MN, Blumberg, B, Carrol, L, Colborn, T, Everett, LG, Hansen, M, Landrigan, PJ, Lanphear, BP, Mesnage, R, Vandenberg, LN, vom Saal, FS, Welshons, WV, Benbrook, CM (2016) Concerns over use of glyphosate-based herbicide and risks associated with exposures: a consensus statement. Environ Health 15:19 CrossRefGoogle ScholarPubMed
Norris, L, Perry, J, Havens, K (2002) A summary of methods for controlling Phragmites australis. Wetl Progr Tech Rep no 02-2 0–8. Williamsburg: Virginia Institute of Marine Science, William & Mary. https://doi.org/10.21220/m2-4xgj-0w83 CrossRefGoogle Scholar
[OMNRF] Ontario Ministry of Natural Resources and Forestry (2017) Invasive Phragmites Control at Long Point Region and Rondeau Provincial Park— Implementation Plan. http://rondeauprovincialpark.ca/wp-content/uploads/2017/09/MNRF_PhragEUR_ImpPlan-2017-_FINAL_September1_2017.pdf Accessed: December 4, 2020Google Scholar
Pearson, DE, Ortega, YK, Runyon, JB, Butler, JL (2016) Secondary invasion: the bane of weed management. Biol Conserv 197:817 CrossRefGoogle Scholar
Peter, CR, Burdick, DM (2010) Can plant competition and diversity reduce the growth and survival of exotic Phragmites australis invading a tidal marsh? Estuar Coast 33:12251236 CrossRefGoogle Scholar
Polowyk, H (2020) Eleocharis geniculata (Bent Spike-Rush) Great Lakes Plains Populations: Conservation in the Face of Invasion. M.Sc thesis. Waterloo, ON, Canada: University of Waterloo. 72 pGoogle Scholar
Pyšek, P, Hulme, PE, Simberloff, D, Bacher, S, Blackburn, TM, Carlton, JT, Dawson, W, Essl, F, Foxcraft, LC, Genocesi, P, Jeschke, JM, Kühn, I, Liebhold, AM, Mandrak, NE, Meyerson, LA, et al. (2020) Scientists’ warning on invasive alien species. Biol Rev. https://doi.org/10.1111/brv.12627 CrossRefGoogle ScholarPubMed
Pyšek, P, Jarošík, V, Hulme, PE, Pergl, J, Hejda, M, Schaffner, U, Montserrat, V (2012) A global assessment of invasive plant impacts on resident species, communities and ecosystems: the interaction of impact measures, invading species’ traits and environment. Global Change Biol 18:17251737 CrossRefGoogle Scholar
Quirion, B, Simek, Z, Dávalos, A, Blossey, B (2017) Management of invasive Phragmites australis in the Adirondacks: a cautionary tale about prospects of eradication. Biol Invasions 20:5973 CrossRefGoogle Scholar
R Core Team (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing Google Scholar
Reznicek, AA, Catling, PM (1989) The flora of Long Point, Regional Municipality of Haldimond-Norfolk, Ontario. Michigan Bot 28:99175 Google Scholar
Robichaud, CD, Rooney, RC (2017) Long-term effects of a Phragmites australis invasion on birds in a Lake Erie coastal marsh. J Great Lakes Res 43:141149 CrossRefGoogle Scholar
Robichaud, CD, Rooney, RC (2021) Low concentrations of glyphosate in water and sediment after direct over-water application to control an invasive aquatic plant. Water Res 188:116573 CrossRefGoogle ScholarPubMed
Rohal, CB, Cranney, C, Hazelton, ELG, Kettenring, KM (2019) Invasive Phragmites australis management outcomes and native plant recovery are context dependent. Ecol Evol 9:1383513849 CrossRefGoogle ScholarPubMed
Saltonstall, K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:24452449 CrossRefGoogle ScholarPubMed
Sesin, V, Davy, CM, Dorken, ME, Gilbert, JM, Freeland, JR (2020) Variation in glyphosate effects and accumulation in emergent macrophytes. Manag Biol Invasions. https://www.reabic.net/journals/mbi/2020/ICAIS/MBI_2020_Sesin_etal_correctedproof.pdf. Accessed: February 8, 2021Google Scholar
Simberloff, D, Martin, J, Genovesi, P, Maris, V, Wardle, DA, Aronson, J, Courchamp, F, Galil, B, Garcia-Berthou, E, Pascal, M, Pyšek, P, Sousa, R, Tabacchi, R, Montserrat, V (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28, https://doi.org/10.1016/j.tree.2012.07.013 CrossRefGoogle Scholar
Simmons, MT (2005) Bullying the bullies: the selective control of an exotic, invasive annual (Rapistrum rugosum) by oversowing with a competitive native species (Gaillardia pulchella). Restor Ecol 13:609615 CrossRefGoogle Scholar
Stoddard, JL, Larsen, DP, Hawkins, CP, Johnson, RK, Norris, RH (2006) Setting expectations for the ecological condition of streams: the concept of reference condition. Ecol Appl 16:12671276 CrossRefGoogle ScholarPubMed
Tozer, DC, Mackenzie, SA (2019) Control of invasive Phragmites increases marsh birds but not frogs. Can Wildlife Biol Manag 8:2 Google Scholar
Turner, RE, Warren, RS (2003) Valuation of continuous and intermittent Phragmites control. Estuaries 26:618623 CrossRefGoogle Scholar
van der Valk, AG (2005) Water-level fluctuations in North American prairie wetlands. Hydrobiologia 539:171188 CrossRefGoogle Scholar
Vera, MS, Lagomarsino, L, Sylvester, M, Pérez, GL, Rodríguez, P, Mugni, H, Sinistro, R, Ferraro, M, Bonetto, C, Zagarese, H, Pizarro, H (2010) New evidences of Roundup® (glyphosate formulation) impact on the periphyton community and the water quality of freshwater ecosystems. Ecotoxicology 19:710721 CrossRefGoogle Scholar
Völlm, C, Tanneberger, F (2014) Shallow inundation favours decomposition of Phragmites australis leaves in a near-natural temperate fen. Mires Peat 14:19 Google Scholar
Vyn, R (2019) Estimated Expenditures on Invasive Species in Ontario: 2019 Survey Results. Sault Ste. Marie, ON, Canada: Invasive Species Centre. https://www.invasivespeciescentre.ca/invasive-species/what-is-at-risk/invasive-species-economic-impacts/. Accessed: May 3, 2020Google Scholar
Whickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. https://cran.r-project.org/web/packages/ggplot2/index.html. Accessed: May 10, 2020Google Scholar
Wikum, DA, Shanholtzer, GF (1978) Application of the Braun-Blanquet cover-abundance scale for vegetation analysis in land development studies. Environ Manag 2:323329 CrossRefGoogle Scholar
Wilcox, KL, Petrie, SA, Maynard, LA, Meyer, SW (2003) Historical distribution and abundance of Phragmites australis at Long Point, Lake Erie, Ontario. J Great Lakes Res 29:664680 CrossRefGoogle Scholar
Yuckin, S (2018) Detecting the Effects of Biological Invasion and Subsequent Control Efforts on Wetland Ecological Processes. M.Sc thesis. Waterloo, ON, Canada: University of Waterloo. 203 pGoogle Scholar
Yuckin, S, Rooney, R (2019) Significant increase in nutrient stocks following Phragmites australis invasion of freshwater meadow marsh but not of cattail marsh. Front Environ Sci 7:116 CrossRefGoogle Scholar
Zhang, L, Zhao, Y, Hein-Griggs, D, Janes, T, Tucker, S, Ciborowski, JJH (2020) Climate change projections of temperature and precipitation for the great lakes basin using the PRECIS regional climate model. J Great Lakes Res 46:255266 CrossRefGoogle Scholar
Zhu, B, Kopco, J, Rudstam, LG (2015) Effects of invasive European frogbit and its two physical control methods on macroinvertebrates. Freshwater Sci 34:497507 CrossRefGoogle Scholar
Zhu, B, Ottaviani, CC, Naddafi, R, Dai, Z, Daolin, D (2018) Invasive European frogbit (Hydrocharis morsus-ranae L.) in North America: an updated review 2003-16. J Plant Ecol 11:1725 CrossRefGoogle Scholar
Zimmerman, CL, Shirer, RR, Corbin, JD (2018) Native plant recovery following three years of common reed (Phragmites australis) control. Invasive Plant Sci Manag 11:175180 CrossRefGoogle Scholar
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