Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-28T19:24:46.184Z Has data issue: false hasContentIssue false
  • English
  • Français

Knotweed (Fallopia spp.) Invasion of North America Utilizes Hybridization, Epigenetics, Seed Dispersal (Unexpectedly), and an Arsenal of Physiological Tactics

Published online by Cambridge University Press:  20 January 2017

Sharon Gillies ,
David R. Clements  and
Jennifer Grenz
Sharon Gillies
Affiliation:
Biology Department, University of the Fraser Valley, 33844 King Road, Abbotsford, Canada V2S 2M8
David R. Clements*
Affiliation:
Department of Biology, Trinity Western University, 7600 Glover Road, Langley, BC, Canada V2Y 1Y1
Jennifer Grenz
Affiliation:
Department of Plant Science, University of British Columbia, 2357 Main Mall 248, Vancouver, BC, Canada V6T 1Z4
*
Corresponding author's E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

More than 100 years ago, Japanese knotweed was introduced to North America. Given its vigorous rhizome system and capability to grow from rhizome and stem fragments, it persists and spreads locally, forming monotypic stands. The Japanese knotweed clone originally introduced was a male sterile female clone; thus, early in the invasion, reproduction from seed was not an issue. The implication was that long-distance dispersal was relatively rare. However, recently, widespread hybridization between Japanese knotweed and Sakhalin (giant) knotweed has been reported, with the hybrid species, Bohemian knotweed, forming the majority of knotweed plants in many areas and possessing higher variability than the parent species. The hybrids produce large numbers of wind-dispersed viable seeds that germinate at rates approaching 100% in some populations. As temperatures increase, knotweed is predicted to expand its range farther north and to higher elevations. With the ability to regenerate from vegetative fragments and disperse via seeds, invasive knotweed species are on the move. An arsenal of chemical weapons, the ability to shade out competitors, and the ability to adapt rapidly through epigenetic change makes knotweed a formidable invader. We observed that knotweed species clearly possess 8 of the 12 ideal weed characteristics, with Bohemian knotweed likely exhibiting still more because of prolific seed production. More research is needed to answer pressing questions. How does hybridization affect knotweed epigenetics? Under what conditions might seed production become more frequent? What kind of niche expansion is possible with the increased variability? Given the considerable challenges posed by knotweed species that promise to become even greater with the proliferation and spread of Bohemian ecotypes, only a thoroughly researched, well-informed approach to knotweed management across North America can be successful.

Keywords

Japanese knotweed, Fallopia japonica (Houtt.) Dcne. syn. Polygonum cuspidatum Sieb. & Zucc.Sakhalin knotweed, Fallopia sachalinensis (F. Schmidt ex Maxim.) Dcne.Bohemian knotweed, Fallopia×bohemica Chrtek & ChrtkovaAllelopathyclonal reproductionepigeneticshybridizationideal weed characteristicsinvasive species
Type
Research Article
Information
Invasive Plant Science and Management , Volume 9 , Issue 1 , March 2016 , pp. 71 - 80
Copyright
Copyright © Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Adachi, N, Terashima, I, Takahaski, M (1996) Central die-back of monoclonal stands of Reynoutria japonica in an early stage of primary succession on Mount Fuji. Ann Bot 77:477–486 Google Scholar
Ainsworth, N, Weiss, J, Jacob, HS, Dodd, J, Moore, JH (2002) Fallopia japonica (Houtt.) Ronse Decr. (Japanese knotweed)—an underrated threat to riparian zones in Australia. Pages 130–133 in Proceedings of 13th Australian Weeds Conference. Perth, WA Council of Australasian Weed Societies Google Scholar
Alder, C (1993) Growth and dispersal strategies and associations of the neophyte Polygonum cuspidatum with special regard to mowing. Tuexenia 13:373–397 Google Scholar
Bailey, JP (1994) The reproductive biology and fertility of Fallopia japonica (Japanese knotweed) and its hybrids in the British Isles. Pages 141–158 in de Waal, C, Child, LE, Wade, M, Brock, JH, eds. Ecology and Management of Invasive Riparian Plants. Chichester, UK Wiley Google Scholar
Bailey, JP, Bímová, K, Mandák, B (2009) Asexual spread versus sexual reproduction and evolution in Japanese Knotweed s.l. sets the stage for the “Battle of the Clones.” Biol Invasions 11:1189–1203 CrossRefGoogle Scholar
Bailey, JP, Conolly, AP (2000) Prize-winners to pariahs—a history of Japanese knotweed s.l. (Polygonaceae) in the British Isles. Watsonia 23:93–110 Google Scholar
Baker, HG (1974) The evolution of weeds. Ann Rev Ecol Sys 5:1–24 Google Scholar
Barney, JN (2006) North American history of two invasive plant species: phytogeographic distribution, dispersal vectors, and multiple introductions. Biol Invasions 8:703–717 Google Scholar
Barney, JN, Tharavil, N, DiTommaso, A, Bhowmik, PC (2006) The biology of invasive alien plants in Canada. 5. Polygonum cuspidatum Sieb. & Zucc. [=Fallopia japonica (Houtt.) Ronse Decr.]. Can J Plant Sci 86:887–905 Google Scholar
Beerling, DJ, Bailey, JP, Conolly, AP (1994) Fallopia japonica (Houtt.) Ronse Decraene. J Ecol 82:959–979 Google Scholar
Beerling, DJ, Huntley, B, Bailey, JP (1995) Climate and the distribution of Fallopia japonica: use of an introduced species to test the predictive capacity of response surfaces. J Veg Sci 6:269–282 CrossRefGoogle Scholar
Berchová-Bímová, K, Soltysiak, J, Vach, M (2014). Role of different taxa and cytotypes in heavy metals absorption in knotweeds (Fallopia ). Sci Agric Bohemica 45:11–18 Google Scholar
Bímová, K, Mandák, B, Pyšek, P (2003) Experimental study of vegetative regeneration in four invasive Reynoutria taxa (Polygonaceae). Plant Ecol 166:1–11 Google Scholar
Bossdorf, O, Richards, CL, Pigliucci, M (2008) Epigenetics for ecologists. Ecol Lett 11:106–115 Google Scholar
Bourchier, RS, Van Hezewijk, BH (2010) Distribution and potential spread of Japanese knotweed (Polygonum cuspidatum) in Canada relative to climatic thresholds. Invasive Plant Sci Manag 3:32–39 Google Scholar
Bram, MR, McNair, JN (2004) Seed germinability and its seasonal onset of Japanese knotweed (Polygonum cuspidatum ). Weed Sci 52:759–767 Google Scholar
Brock, JH, Child, LE, de Waal, LD, Wade, M, Pyšek, P, Prach, K, Rejmánek, M (1995) The invasive nature of Fallopia japonica is enhanced by vegetative regeneration from stem tissues. Pages 131–139 in Plant Invasions: General Aspects and Special Problems. Workshop held at Kostelec nad Černými lesy, Czech Republic, September 16–19, 1993. Amsterdam, Netherlands SPB Academic Publishing Google Scholar
Bzdęga, K, Janiak, A, Tarłowska, S, Kurowska, M, Tokarska-Guzik, B, Szarejko, I (2012) Unexpected genetic diversity of Fallopia japonica from Central Europe revealed after AFLP analysis. Flora 207:636–645 CrossRefGoogle Scholar
Chaney, L, Baucom, RS (2012) The evolutionary potential of Baker's weediness traits in the common morning glory, Ipomoea purpurea (Convolvulaceae). Am J Bot 99:1524–1530 Google Scholar
Chiba, N, Hirose, T (1993) Nitrogen acquisition and use in three perennials in the early stage of primary succession. Funct Ecol 7:287–292 Google Scholar
Claeson, SM, Bisson, PA (2013) Passive reestablishment of riparian vegetation following removal of invasive knotweed (Polygonum ). Invasive Plant Sci Manag 6:208–218 Google Scholar
Clements, DR, DiTommaso, A (2012) Predicting weed invasion in Canada under climate change: evaluating evolutionary potential. Can J Plant Sci 92:1013–1020 Google Scholar
Clements, DR, DiTommaso, A, Hyvönen, T (2014) Ecology and management of weeds in a changing climate. Pages 13–37 in Chauhan, BS, Mahajan, G. Recent Advances in Weed Management. Berlin, Germany Springer. 411 pGoogle Scholar
Clements, DR, Larsen, T, Grenz, J (2016) Knotweed management strategies in North America with the advent of widespread hybrid Bohemian knotweed, regional differences, and the potential for biocontrol via the psyllid Aphalara itadori Shinji. Invasive Plant Sci Manag 9:60–70 CrossRefGoogle Scholar
Colleran, BP, Goodall, KE (2014) In situ growth and rapid response management of flood-dispersed Japanese knotweed (Fallopia japonica ). Invasive Plant Sci Manag 7:84–92 Google Scholar
Dommanget, F, Evette, A, Spiegelberger, T, Gallet, C, Pace, M, Imbert, M, Navas, ML (2014) Differential allelopathic effects of Japanese knotweed on willow and cottonwood cuttings used in riverbank restoration techniques. J Environ Manage 132:71–78 Google Scholar
Douhovnikoff, V, Dodd, RS (2015) Epigenetics: a potential mechanism for clonal plant success. Plant Ecol 216:227–223Google Scholar
Duquette, M-C, Compérot, A, Hayes, LF, Pagola, C, Belzile, F, Dubé, Lavoie C (2015) From the source to the outlet: understanding the distribution of invasive knotweeds along a North American River. River Res Appl. DOI: 10.1002/rra.2914CrossRefGoogle Scholar
Engler, J, Abt, K, Buhk, C (2011) Seed characteristics and germination limitations in the highly invasive Fallopia japonica s.l. (Polygonaceae). Ecol Res 26:555–562 Google Scholar
Forman, J, Kesseli, RV (2003) Sexual reproduction in the invasive species Fallopia japonica (Polygonaceae). Am J Bot 90:586–592 CrossRefGoogle ScholarPubMed
Gammon, MA, Baack, E, Orth, JF, Kesseli, R (2010) Viability, growth, and fertility of knotweed cytotypes in North America. Invasive Plant Sci Manag 3:208–218 Google Scholar
Gammon, MA, Grimsby, JL, Tsirelson, D, Kesseli, R (2007) Molecular and morphological evidence reveals introgression in swarms of the invasive taxa Fallopia japonica, F. sachalinensis, and F.× bohemica (Polygonaceae) in the United States. Am J Bot 94:948–956 Google Scholar
Gaskin, JF, Schwarzländer, M, Grevstad, FS, Haverhals, MA, Bourchier, RS, Miller, TW (2014) Extreme differences in population structure and genetic diversity for three invasive congeners: knotweeds in western North America. Biol Invasions 16:2127–2136 Google Scholar
Gerber, E, Krebs, C, Murrell, C, Moretti, M, Rocklin, R, Schaffner, U (2008) Exotic invasive knotweeds (Fallopia spp.) negatively affect native plant and invertebrate assemblages in European riparian habitats. Biol Conserv 141:646–654 CrossRefGoogle Scholar
Grimsby, JL, Kesseli, R (2010) Genetic composition of invasive Japanese knotweed s.l. in the United States. Biol Invasions 12:1943–1946 Google Scholar
Grimsby, JL, Tsirelson, D, Gammon, MA, Kesseli, R (2007) Genetic diversity and clonal vs. sexual reproduction in Fallopia spp. (Polygonaceae). Am J Bot 94:957–964 Google Scholar
Groeneveld, E, Belzile, F, Lavoie, C (2014) Sexual reproduction of Japanese knotweed (Fallopia japonica s.l.) at its northern distribution limit: new evidence of the effect of climate warming on an invasive species. Am J Bot 101:459–466 Google Scholar
Heděnec, P, Novotný, D, Ust'ak, S, Honzík, R, Kovářová, M, Šimáčková, H, Frouz, J (2014) Allelopathic effect of new introduced biofuel crops on the soil biota: a comparative study. Eur J Soil Biol 63:14–20 Google Scholar
Herpigny, B, Dassonville, N, Ghysels, P, Mahy, G, Meerts, P (2012) Variation of growth and functional traits of invasive knotweeds (Fallopia spp.) in Belgium. Plant Ecol 213:419–430 CrossRefGoogle Scholar
Hollingsworth, ML, Bailey, JP (2000) Evidence for massive clonal growth in the invasive weed Fallopia japonica (Japanese knotweed). Bot J Linn Soc 133:463–472 Google Scholar
Inderjit, Callaway RM (2003) Experimental designs for the study of allelopathy. Plant Soil 256:1–11 Google Scholar
Kilvitis, HJ, Alvarez, M, Foust, CM, Schrey, AW, Robertson, M, Richards, CL (2014) Ecological epigenetics. Pages 191–210 in Landry CR, Aubin-Horth N, eds. Ecological Genomics. The Netherlands Springer Google Scholar
Krebs, C, Gerber, E, Matthies, D, Schaffner, U (2011) Herbivore resistance of invasive Fallopia species and their hybrids. Oecologia 167:1041–1052 Google Scholar
Krebs, C, Mahy, G, Matthies, D, Schaffner, U, Tiébré, MS, Bizoux, JP (2010) Taxa distribution and RAPD markers indicate different origin and regional differentiation of hybrids in the invasive Fallopia complex in central-western Europe. Plant Biol 12:215–223 Google Scholar
Lau, JA, Puliafico, KP, Kopshever, JA, Steltzer, H, Jarvis, EP, Schwarzländer, M, Straus, SY, Hufbauer, RA (2008) Inference of allelopathy is complicated by effects of activated carbon on plant growth. New Phytol 178:412–423 Google Scholar
Lecerf, A, Patfield, D, Boiché, A, Riipinen, MP, Chauvet, E, Dobson, M (2007) Stream ecosystems respond to riparian invasion by Japanese knotweed (Fallopia japonica ). Can J Fish Aquat Sci 64:1273–1283 CrossRefGoogle Scholar
Lorenzo, P, Hussain, MI, González, L (2013) Role of allelopathy during invasion process by alien invasive plants in terrestrial ecosystems. Pages 3–21 in Cheema, ZA, Farooq, M, Wahid, A, eds. Allelopathy. Heidelberg, Germany Springer CrossRefGoogle Scholar
Lowe, S, Browne, M, Boudjelas, S, De Poorter, M (2000) 100 of the World's Worst Invasive Alien Species: A Selection from the Global Invasive Species Database. Auckland, New Zealand Invasive Species Specialist Group. P 12 Google Scholar
Maerz, JC, Blossey, B, Nuzzo, V (2005) Green frogs show reduced foraging success in habitats invaded by Japanese knotweed. Biodivers Conserv 14:2901–2911 Google Scholar
Maerz, JC, Nuzzo, VA, Blossey, B (2009) Declines in woodland salamander abundance associated with non-native earthworm and plant invasions. Conserv Biol 23:975–981 Google Scholar
Maruta, E (1983) Growth and survival of current-year seedlings of Polygonum cuspidatum at the upper distribution limit on Mt. Fuji. Oecologia 60:316–320 Google Scholar
Moravcová, L, Pyšek, P, Vojtěch, J, Havlíčová, V, Zákravský, P (2010) Reproductive characteristics of neophytes in Czech Republic: traits of invasive and non-invasive species. Preslia 82:365–390 Google Scholar
Murrell, C, Gerber, E, Krebs, C, Parepa, M., Schaffner, U, Bossdorf, O (2011) Invasive knotweed affects native plants through allelopathy. Am J Bot 98:38–43 Google Scholar
Nishitani, S, Masuzawa, T (1996) Germination characteristics of two species of Polygonum in relation to their altitudinal distribution on Mt. Fuji, Japan. Arct Alp Res 28:104–110 Google Scholar
Parepa, M, Fischer, M, Krebs, C, Bossdorf, O (2014) Hybridization increases invasive knotweed success. Evol Appl 7:413–420 Google Scholar
Parepa, M, Schaffner, U, Bossdorf, O (2013) Help from under ground: soil biota facilitate knotweed invasion. Ecosphere 4:31.CrossRefGoogle Scholar
Parepa, M, Schaffner, U, Bossdorf, O (2012) Sources and modes of action of invasive knotweed allelopathy: the effects of leaf litter and trained soil on the germination and growth of native plants. Neobiota 13:15–30 Google Scholar
Piola, F, Bellvert, F, Meiffren, G, Rouifed, S, Walker, V, Comte, G, Bertrand, C (2013) Invasive Fallopia × bohemica interspecific hybrids display different patterns in secondary metabolites. Ecoscience 20:230–239 Google Scholar
Rahmonov, O, Czylok, A, Orczewska, A, Majgier, L, Parusel, T (2014) Chemical composition of the leaves of Reynoutria japonica Houtt. and soil features in polluted areas. Cent Eur J Biol 9:320–330 Google Scholar
Rapp, RA, Wendel, JF (2005) Epigenetics and plant evolution. New Phytol 168:81–91 Google Scholar
Rice, EL (1984) Allelopathy. New York, NY Academic Press. 368 pGoogle Scholar
Richards, CL, Schrey, AW, Pigliucci, M (2012) Invasion of diverse habitats by few Japanese knotweed genotypes is correlated with epigenetic differentiation. Ecol Lett 15:1016–1025 CrossRefGoogle ScholarPubMed
Richards, CL, Walls, RL, Bailey, JP, Parameswaran, R, George, T, Pigliucci, M (2008) Plasticity in salt tolerance traits allows for invasion of novel habitat by Japanese knotweed s.l. (Fallopia japonica and F. × bohemica, Polygonaceae). Am J Bot 95:931–942 Google Scholar
Rouifed, S, Byczek, S, Laffray, D, Piola, F (2012) Invasive knotweeds are highly tolerant to salt stress. Environ Manag 50:1027–1034 Google Scholar
Rouifed, S, Puijalon, S, Viricel, MR, Piola, F (2011) Achene buoyancy and germinability of the terrestrial invasive Fallopia × bohemica in aquatic environment: a new vector of dispersion? Ecoscience 18:79–84 CrossRefGoogle Scholar
Schrey, AW, Alvarez, M, Foust, CM, Kilvitis, HJ, Lee, JD, Liebl, AL, Robertson, M (2013) Ecological epigenetics: beyond MS-AFLP. Integr Comp Biol 53:340–350 Google Scholar
Seiger, L (1984) The Ecology and Control of Reynoutria japonica (Polygonum cuspidatum). Ph.D dissertation. Washington, DC George Washington University. 117 pGoogle Scholar
Šerá, B (2012) Effects of soil substrate contaminated by knotweed leaves on seed development. Pol J Environ Stud 21:713–717 Google Scholar
Siemens, TJ, Blossey, B (2007) An evaluation of mechanisms preventing growth and survival of two native species in invasive Bohemian knotweed (Fallopia × bohemica, Polygonaceae). Am J Bot 94:776–783 Google Scholar
Sołtysiak, J, Brej, T (2012) Characteristics that make the Fallopia genus (Polygonaceae) highly invasive. Ecol Questions 16:23–27 Google Scholar
Stoll, P, Gatzsch, K, Rusterholz, HP, Baur, B (2012) Response of plant and gastropod species to knotweed invasion. Basic Appl Ecol 13:232–240 Google Scholar
Sukopp, H, Starfinger, U, Pyšek, P, Prach, K, Rejmánek, M, Wade, M (1995) Reynoutria sachalinensis in Europe and in the Far East: a comparison of the species ecology in its native and adventive distribution range. Pages 151–159 in Plant Invasions: General Aspects and Special Problems. Workshop held at Kostelec nad Černými lesy, Czech Republic, September 16–19, 1993. Amsterdam, Netherlands SPB Academic Publishing Google Scholar
Tiébré, MS, Saad, L, Mahy, G (2008) Landscape dynamics and habitat selection by the alien invasive Fallopia (Polygonaceae) in Belgium. Biodivers Conserv 17:2357–2370 Google Scholar
Tiébré, MS, Vanderhoeven, S, Saad, L, Mahy, G (2007) Hybridization and sexual reproduction in the invasive alien Fallopia (Polygonaceae) complex in Belgium. Ann Bot 99:193–203 CrossRefGoogle ScholarPubMed
Toews, HPC (2012) Introduction of Native Tree Species in Sites Invaded by Japanese Knotweed Taxa and a Study of its Effects on the Seedbank. M.Sc dissertation. Fredonia, NY New York State University. 41 pGoogle Scholar
Topp, W, Kappes, H, Rogers, F (2008) Response of ground-dwelling beetle (Coleoptera) assemblages to giant knotweed (Reynoutria spp.) invasion. Biol Invasions 10:381–390 Google Scholar
Urgenson, LS, Reichard, SH, Halpern, CB (2009) Community and ecosystem consequences of giant knotweed (Polygonum sachalinense) invasion into riparian forests of western Washington, USA. Biol Conserv 142:1536–1541 Google Scholar
Urgenson, LS, Reichard, SH, Halpern, CB (2014) Habitat factors and species’ traits influence riparian community recovery following removal of Bohemian knotweed (Polygonum × bohemicum ). Northwest Sci 88:246–260 Google Scholar
[USDA-NRCS] U.S. Department of Agriculture Natural Resources Conservation Service. 2015. The PLANTS Database. http://plants.usda.gov. Accessed February 1, 2015Google Scholar
Vanderhoeven, S, Dassonville, N, Meerts, P (2005) Increased topsoil mineral nutrients concentrations under exotic invasive plants in Belgium. Plant Soil 275:169–179 Google Scholar
Verhoeven, KJ, Jansen, JJ, van Dijk, PJ, Biere, A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108–1118 Google Scholar
Vrchotová, N, Šerá, B (2008) Allelopathic properties of knotweed rhizome extracts. Plant Soil Environ 54:301–303 Google Scholar
Weißhuhn, PD (2009) Activated carbon may have undesired side effects for testing allelopathy in invasive plants. Basic Appl Ecol 10:500–507 Google Scholar