Evidence does not support the targeting of cryptic invaders at the subspecies level using classical biological control: the example of Phragmites

Abstract

Classical biocontrol constitutes the importation of natural enemies from a native range to control a non-native pest. This is challenging when the target organism is phylogenetically close to a sympatric non-target form. Recent papers have proposed and recommended that two European moths (Archanara spp.) be introduced to North America to control non-native Phragmites australis australis, claiming they would not adversely affect native P. australis americanus. We assert that these papers overlooked research contradicting their conclusions and that the authors recommended release of the non-native moths despite results of their own studies indicating that attack on native Phragmites is possible after field release. Furthermore, their open-field, host-specificity tests were conducted in non-wetland fields in Switzerland using potted plants, reflecting considerably different conditions than those of North American wetlands. Also, native Phragmites in eastern North America has declined, increasing its potential vulnerability to any new stressors. Because all inadvertently introduced, established, Phragmites-specialist, herbivorous insects have done more harm to native than non-native Phragmites, native Phragmites may experience more intense herbivory than non-native Phragmites from the introduction of Archanara spp. due to demographic mechanisms (e.g., increase in density of the biocontrol agent and spillover onto alternate hosts) or because the herbivores may undergo genetic change. In addition to the risk to native Phragmites, significant biomass reduction of non-native Phragmites may decrease important ecosystem services, including soil accretion in wetlands affected by sea level rise. We strongly caution against the approval of Archanara spp. as biocontrol agents for non-native Phragmites in North America.

This is a preview of subscription content, access via your institution.

References

  1. Allen WJ, Young RE, Bhattarai GP, Croy JR, Lambert AM, Meyerson LA, Cronin JT (2015) Multitrophic enemy escape of invasive Phragmites australis and its introduced herbivores in North America. Biol Invasions 17:3419–3432

    Article  Google Scholar 

  2. Allen GA, McCormick LJ, Jantzen JR, Marr KL, Brown BN (2017a) Distributional and morphological differences between native and introduced common reed (Phragmites australis, Poaceae) in western Canada. Wetlands 37:819–827

    Article  Google Scholar 

  3. Allen WJ, Meyerson LA, Cummings D, Anderson J, Bhattarai GP, Cronin JT (2017b) Biogeography of a plant invasion: drivers of latitudinal variation in local enemy release. Glob Ecol Biogeogr 26:435–446

    Article  Google Scholar 

  4. Andres LA (1985) Interaction of Chrysolina quadrigemina and Hypericum spp. in California. In: Delfosse ES (ed) Proceedings of the VI international symposium on biological control of weeds, August 1984, Agriculture Canada, Vancouver, pp 235–239

  5. Araujo SBL, Pires Braga M, Brooks DR, Agosta SJ, Hoberg EP, von Hartenthal FW, Boeger WA (2015) Understanding host-switching by ecological fitting. PLoS ONE 10:e0139225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81(2):169–193

    Article  Google Scholar 

  7. Begg JS, Lavigne RL, Veneman PLM (2001) Reed beds: constructed wetlands for municipal wastewater treatment plant sludge dewatering. Water Sci Technol 44:393–398

    Article  CAS  PubMed  Google Scholar 

  8. Bernal B, Megongal JP, Mozdzer TJ (2016) An invasive wetland grass primes deep soil carbon pools. Glob Chang Biol 23(5):2104–2116

    Article  PubMed  Google Scholar 

  9. Bhattarai GP, Allen WJ, Cronin JT, Kiviat E, Meyerson LA (2016) Response to Blossey and Casagrande—ecological and evolutionary processes make host specificity at the subspecies level exceedingly unlikely. Biol Invasions 18:2757–2758

    Article  Google Scholar 

  10. Bhattarai GP, Meyerson LA, Anderson J, Cummings D, Allen WJ, Cronin JT (2017a) Biogeography of a plant invasion: genetic variation and plasticity in latitudinal clines for traits related to herbivory. Ecol Monogr 87:57–75

    Article  Google Scholar 

  11. Bhattarai GP, Meyerson LA, Cronin JT (2017b) Geographic variation in apparent competition between native and invasive Phragmites australis. Ecology 98(2):349–358

    Article  PubMed  Google Scholar 

  12. Blossey B (2003) A framework for evaluating potential ecological effects of implementing biological control of Phragmites australis. Estuaries 26:607–617

    Article  Google Scholar 

  13. Blossey B (2014) Identification, development, and release of insect biocontrol agents for the management of Phragmites australis. ERDC/EL CR-14-2. US Army Corps of Engineers, Washington

    Google Scholar 

  14. Blossey B, Casagrande RA (2016a) Biological control of invasive Phragmites may safeguard native Phragmites and increase wetland conservation values. Biol Invasions 18(9):2753–2755

    Article  Google Scholar 

  15. Blossey B, Casagrande RA (2016b) Response to Bhattarai et al.: trait differences between native and introduced genotypes results in subspecies level specificity in select Phragmites herbivores. Biol Invasions 18:2759–2760

    Article  Google Scholar 

  16. Blossey B, McCauley J (2000) A plan for developing biological control of Phragmites australis in North America. Wetl J 12:23–28

    Google Scholar 

  17. Blossey B, Casagrande RA, Tewksbury L, Hinz H, Häfliger P, Martin L, Cohen J (2013) Identifying, developing and releasing insect biocontrol agents for the management of Phragmites australis. ERDC/EL TN-13-3. U.S. Army Engineer Research and Development Center, Vicksburg

    Google Scholar 

  18. Blossey B, Häfliger P, Tewksbury L, Dávalos A, Casagrande R (2018a) Host specificity and risk assessment of Archanara geminipuncta and Archanara neurica, two potential biocontrol agents for invasive Phragmites australis in North America. Biol Control 125:98–112

    Article  Google Scholar 

  19. Blossey B, Häfliger P, Tewksbury L, Dávalos A, Casagrande R (2018b) Complete host specificity test plant list and associated data to assess host specificity of Archanara geminipuncta and Archanara neurica, two potential biocontrol agents for invasive Phragmites australis in North America. Data in Brief 19:1755–1764. https://doi.org/10.1016/j.dib.2018.06.068

    Article  PubMed  PubMed Central  Google Scholar 

  20. Buswell JM, Moles AT, Hartley S (2010) Is rapid evolution common in introduced plant species? J Ecol 99:214–224

    Article  Google Scholar 

  21. Caplan JS, Hager RN, Megonigal JP, Mozdzer TJ (2015) Global change accelerates carbon assimilation by a wetland ecosystem engineer. Environ Res Lett 10:115006. https://doi.org/10.1088/1748-9326/10/11/115006

    CAS  Article  Google Scholar 

  22. Carroll S, Boyd C (1992) Host race radiation in the soapberry bug—natural history with the history. Evolution 46:1052–1069

    Article  PubMed  Google Scholar 

  23. Casagrande RA, Häfliger P, Hinz HL, Tewksbury L, Blossey B (2018) Grasses as appropriate targets in weed biocontrol: is the common reed, Phragmites australis, an anomaly? Biocontrol 63:391–403. https://doi.org/10.1007/s10526-018-9871-y

    Article  Google Scholar 

  24. Castagneyrol B, Jactel H, Brockerhoff EG, Perrette N, Larter M, Delzon S, Piou D (2016) Host range expansion is density dependent. Oecologia 182:779–788

    Article  PubMed  Google Scholar 

  25. Cenzer ML (2016) Adaptation to an invasive host is driving the loss of a native ecotype. Evolution 70:2296–2307

    Article  PubMed  Google Scholar 

  26. Ciotir C, Kirk H, Row JR, Freeland JR (2013) Intercontinental dispersal of Typha angustifolia and T. latifolia between Europe and North America has implications for Typha invasions. Biol Invasions 15:1377–1390

    Article  Google Scholar 

  27. Cipollini D, Peterson DL (2018) The potential for host switching via ecological fitting in the emerald ash borer-host plant system. Oecologia 187:507–519

    Article  PubMed  Google Scholar 

  28. Colin R, Eguiarte LE (2016) Phylogeographic analyses and genetic structure illustrate the complex evolutionary history of Phragmites australis in Mexico. Am J Bot 103(5):876–887

    Article  CAS  PubMed  Google Scholar 

  29. Cronin JT, Bhattarai GP, Allen WJ, Meyerson LA (2015) Biogeography of a plant invasion: plant-herbivore interactions. Ecology 96:1115–1127

    Article  PubMed  Google Scholar 

  30. Cronin JT, Kiviat E, Meyerson LA, Bhattarai GP, Allen WJ (2016) Biological control of invasive Phragmites australis will be detrimental to native P. australis. Biol Invasions 18:2749–2752

    Article  Google Scholar 

  31. Des Roches S, Post DM, Turley NE, Bailey JK, Hendry AP, Kinnison MT, Schweitzer JA, Palkovacs EP (2018) The ecological importance of intraspecific variation. Nat Ecol Evol 2:57–64

    Article  PubMed  Google Scholar 

  32. Desurmont GA, Donoghue MJ, Clement WL, Agrawal AA (2011) Evolutionary history predicts plant defense against an invasive pest. Proc Natl Acad Sci 108:7070–7074

    Article  PubMed  Google Scholar 

  33. Dingle H, Carroll SP, Famula TR (2009) Influence of genetic architecture on contemporary local evolution in the soapberry bug, Jadera haematoloma: artificial selection on beak length. J Evol Biol 22:2031–2040

    Article  CAS  PubMed  Google Scholar 

  34. Erbilgin N, Ma C, Whitehouse C, Shan B, Najar A, Evenden M (2014) Chemical similarity between historical and novel host plants promotes range and host expansion of the mountain pine beetle in a naïve host ecosystem. New Phytol 201:940–950

    Article  PubMed  Google Scholar 

  35. Floate KD, Whitham TG (1993) The hybrid bridge hypothesis—host shifting via plant hybrid swarms. Am Nat 141:651–662

    Article  CAS  Google Scholar 

  36. Floate KD, Kaersley MJC, Whitham TG (1993) Elevated herbivory in plant hybrid zone: Chrysomela confluens, Populus and phenological sinks. Ecology 74:2056–2065

    Article  Google Scholar 

  37. Gaskin JF, Schaal BA (2002) Hybrid Tamarix widespread in U.S. invasion and undetected in native Asian range. Proc Natl Acad Sci 99:11256–11259

    Article  CAS  PubMed  Google Scholar 

  38. Gilbert GS, Briggs HM, Magarey R (2015) The impact of plant enemies shows a phylogenetic signal. PLoS ONE. https://doi.org/10.1371/journal.pone.0123758

    Article  PubMed  PubMed Central  Google Scholar 

  39. Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Conserv 110:413–433

    Article  Google Scholar 

  40. Grosholz E (2010) Avoidance by grazers facilitates spread of an invasive hybrid plant. Ecol Lett 13:145–153

    Article  CAS  PubMed  Google Scholar 

  41. Guo W-Y, Lambertini C, Nguyen LX, Li X-Z, Brix H (2014) Preadaptation and post-introduction evolution facilitate the invasion of Phragmites australis in North America. Ecol Evol 4:4567–4577

    Article  PubMed  PubMed Central  Google Scholar 

  42. Guo W-Y, Lambertini C, Pyšek P, Meyerson LA, Brix H (2018) Living in two worlds: evolutionary mechanisms act differently in the native and introduced ranges of an invasive plant. Ecol Evol 8:2440–2452

    Article  PubMed  PubMed Central  Google Scholar 

  43. Häfliger P, Schwarzländer M, Blossey B (2006) Impact of Archanara geminipuncta (Lepidoptera: Noctuidae) on aboveground biomass production of Phragmites australis. Biol Control 38:413–421

    Article  Google Scholar 

  44. Hallgren P, Ikonen A, Hjaelte J, Roininen H (2003) Inheritance patterns of phenolics in F1, F2 and back-cross hybrids of willows: implications for herbivore responses to hybrid plants. J Chem Ecol 29:1143–1158

    Article  CAS  PubMed  Google Scholar 

  45. Hazelton EL, 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:plu001. https://doi.org/10.1093/aob-pla/plu001

    Article  PubMed  PubMed Central  Google Scholar 

  46. Heimpel GE, Cock MJW (2018) Shifting paradigms in the history of classical biological control. Biocontrol 63:27–37

    Article  Google Scholar 

  47. Hershner C, Havens KJ (2008) Managing invasive aquatic plants in a changing system: strategic consideration of ecosystem services. Conserv Biol 22(3):544–550

    Article  PubMed  Google Scholar 

  48. Kane R (2001) Phragmites use by birds in New Jersey. Rec New Jersey Birds 26:122–124

    Google Scholar 

  49. Kettenring KM, Mock KE (2012) Genetic diversity, reproductive mode, and dispersal differ between the cryptic invader, Phragmites australis, and its native conspecific. Biol Invasions 14:2489–2504

    Article  Google Scholar 

  50. Kirwan ML, Temmerman S, Skeehan EE, Guntenspergen GR, Fagherazzi S (2016) Overestimation of marsh vulnerability to sea level rise. Nat Clim Chang 6(3):253–260

    Article  Google Scholar 

  51. Kiviat E (2013) Ecosystem services of Phragmites in North America with emphasis on habitat functions. AoB PLANTS 5:plt008. https://doi.org/10.1093/aobpla/plt00

    Article  PubMed Central  Google Scholar 

  52. Kiviat E, Hamilton E (2001) Phragmites use by Native North Americans. Aquat Bot 69(2–4):341–357

    Article  Google Scholar 

  53. Knight IA, Wilson BE, Gill M, Aveles L, Cronin JT, Nyman JA, Schneider SA, Diaz R (2018) Invasion of Nipponaclerda biwakoensis (Hemiptera: Aclerdidae) and associated Phragmites australis dieback in southern Louisiana. Biol Invasions 20:2739–2744

    Article  Google Scholar 

  54. Kulmatiski A, Beard KH, Meyerson LA, Gibson JR, Mock KE (2011) Nonnative Phragmites australis invasion into Utah wetlands. West N Am Nat 70(4):541–552

    Article  Google Scholar 

  55. Lambert AM, Casagrande RA (2007) Susceptibility of native and non-native common reed to the non-native mealy plum aphid (Homoptera: Aphididae) in North America. Environ Entomol 36:451–457

    Article  PubMed  Google Scholar 

  56. Lambert AM, Winiarski K, Casagrande RA (2007) Distribution and impact of exotic gall flies (Lipara sp. [sic]) on native and exotic Phragmites australis. Aquat Bot 86:163–170

    Article  Google Scholar 

  57. Lambertini C (2016) Heteroplasmy due to chloroplast paternal leakage: another insight into Phragmites haplotypic diversity in North America. Biol Invasions 18:2443–2455

    Article  Google Scholar 

  58. Lambertini C, Gustafsson MHG, Frydenberg J, Lissner J, Speranza M, Brix H (2006) A phylogeographic study of the cosmopolitan genus Phragmites (Poaceae) based on AFLPs. Plant Syst Evol 258(3–4):161–182

    Article  Google Scholar 

  59. Lambertini C, Mendelssohn IA, Gustafsson MHG, Olesen B, Riis T, Sorrell BK, Brix H (2012) Tracing the origin of Gulf Coast Phragmites (Poaceae): a story of long-distance dispersal and hybridization. Am J Bot 99:538–551

    Article  CAS  PubMed  Google Scholar 

  60. Long J, Tecle A, Burnette B (2003) Cultural foundations for ecological restoration on the White Mountain Apache Reservation. Conserv Ecol 8(1). Available via Ecology and Society http://www.consecol.org/vol8/iss1/art4

  61. Louda SM, Arnett AE, Rand TA, Russell FL (2003) Invasiveness of some biological control insects and adequacy of their ecological risk assessment and regulation. Conserv Biol 17(1):73–82

    Article  Google Scholar 

  62. Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280

    Article  Google Scholar 

  63. McCormick MK, Kettenring KM, Baron HM, Whigham DF (2010) Spread of invasive Phragmites australis in estuaries with differing degrees of development: genetic patterns, Allee effects and interpretation. J Ecol 98:1369–1378

    Article  Google Scholar 

  64. Meyerson LA, Cronin JT (2013) Evidence for multiple introductions of Phragmites australis to North America: detection of a new non-native haplotype. Biol Invasions 15:2605–2608

    Article  Google Scholar 

  65. Meyerson LA, Mooney HA (2007) Invasive alien species in an era of globalization. Front Ecol Environ 5:199–208

    Article  Google Scholar 

  66. Meyerson LA, Saltonstall K, Windham L, Kiviat E, Findlay S (2000) A comparison of Phragmites australis in freshwater and brackish marsh environments in North America. Wetl Ecol Manag 8:89–103

    Article  CAS  Google Scholar 

  67. Meyerson LA, Saltonstall K, Chambers RM (2009) Phragmites australis in eastern North America: a historical and ecological perspective. In: Silliman BR, Grosholz E, Bertness MD (eds) Salt marshes under global siege. University of California Press, Oakland

    Google Scholar 

  68. Meyerson LA, Lambert AM, Saltonstall K (2010a) A tale of three lineages: expansion of common reed (Phragmites australis) in the U.S. Southwest and Gulf Coast. Invasive Plant Sci Manag 3:515–520

    Article  Google Scholar 

  69. Meyerson LA, Viola D, Brown R (2010b) Hybridization of invasive Phragmites australis with a native subspecies in North America. Biol Invasions 12:103–111

    Article  Google Scholar 

  70. Meyerson LA, Lambertini C, McCormick M, Whigham DF (2012) Hybridization of common reed in North America? The answer is blowing in the wind. AoB PLANTS 2012:pls1022. https://doi.org/10.1093/aobpla/pls1022

    Article  Google Scholar 

  71. Meyerson LA, Cronin JT, Bhattarai GP, Brix H, Lambertini C, Lučanová M, Rinehart S, Suda J, Pyšek P (2016a) Do ploidy level and nuclear genome size and latitude of origin modify the expression of Phragmites australis traits and interactions with herbivores? Biol Invasions 18:2531–2549

    Article  Google Scholar 

  72. Meyerson LA, Cronin JT, Pyšek P (2016b) Phragmites australis as a model organism for studying plant invasions. Biol Invasions 18:2421–2431

    Article  Google Scholar 

  73. Mozdzer TJ, Zieman JC (2010) Ecophysiological differences between genetic lineages facilitate the invasion of non-native Phragmites australis in North American Atlantic coast wetlands. J Ecol 98:451–458

    Article  Google Scholar 

  74. Mozdzer TJ, Zieman JC, McGlathery KJ (2010) Nitrogen uptake by native and invasive temperate coastal macrophytes: importance of dissolved organic nitrogen. Estuaries Coasts 33:784–797

    Article  CAS  Google Scholar 

  75. Mozdzer TJ, Brisson J, Hazelton EL (2013) Physiological ecology and functional traits of North American native and Eurasian introduced Phragmites australis lineages. AoB Plants 5:plt048. https://doi.org/10.1093/aobpla/plt048

    Article  PubMed Central  Google Scholar 

  76. Murdoch WW (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol Monogr 39:335–354

    Article  Google Scholar 

  77. Nelson MF, Anderson NO, Casler MD, Jakubowski AR (2014) Population genetic structure of N. American and European Phalaris arundinacea L. as inferred from inter-simple sequence repeat markers. Biol Invasions 16(2):353–363

    Article  Google Scholar 

  78. Packer J, Meyerson LA, Skálová H, Pyšek P, Kueffer C (2017) Biological flora of the British Isles: Phragmites australis. J Ecol 105:1123–1162

    Article  Google Scholar 

  79. Park MG, Blossey B (2008) Importance of plant traits and herbivory for invasiveness of Phragmites australis (Poaceae). Am J Bot 95:1557–1568

    Article  PubMed  Google Scholar 

  80. Parker IM, Saunders M, Bontrager M, Weitz AP, Hendricks R, Magarey R, Suiter K, Gilbert GS (2015) Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520:542–544

    Article  CAS  PubMed  Google Scholar 

  81. Paul J, Vachon N, Garroway CJ, Freeland JR (2010) Molecular data provide strong evidence of natural hybridization between native and introduced lineages of Phragmites australis in North America. Biol Invasions 12:2967–2973

    Article  Google Scholar 

  82. Paynter Q, Fowler SV, Gourlay AH, Peterson PG, Smith LA, Winks CJ (2015) Relative performance on test and target plants in laboratory tests predicts the risk of non-target attack in the field for arthropod weed biocontrol agents. Biol Control 80:133–142

    Article  Google Scholar 

  83. Pearse IS, Altermatt F (2013) Predicting novel trophic interactions in a non-native world. Ecol Lett 16:1088–1094

    Article  PubMed  Google Scholar 

  84. Pearse IS, Hipp AL (2009) Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks. Proc Natl Acad Sci 106:18097–18102

    Article  PubMed  Google Scholar 

  85. Pearse IS, Harris DJ, Karban R, Sih A (2013) Predicting novel herbivore-plant interactions. Oikos 122:1554–1564

    Article  Google Scholar 

  86. Pearson DE, Callaway RM (2005) Indirect nontarget effects of host-specific biological control agents: implications for biological control. Biol Control 35:288–298

    Article  Google Scholar 

  87. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294

    Article  CAS  PubMed  Google Scholar 

  88. Ravit B, Weis JS, Rounds D (2015) Is urban marsh sustainability compatible with the Clean Water Act? Environ Pract 17(1):46–56

    Article  Google Scholar 

  89. Rodríguez M, Brisson J (2015) Pollutant removal efficiency of native versus exotic common reed (Phragmites australis) in North American treatment wetlands. Ecol Eng 74:364–370

    Article  Google Scholar 

  90. Rooth JE, Stevenson JC (2000) Sediment deposition patterns in Phragmites australis communities: implications for coastal areas threatened by rising sea level. Wetl Ecol Manag 8:173–183

    Article  Google Scholar 

  91. Rooth JE, Windham L (2000) Phragmites on death row: is biocontrol really warranted? Wetl J 12:29–37

    Google Scholar 

  92. Rooth JE, Stevenson JC, Cornwell JC (2003) Increased sediment accretion rates following invasion by Phragmites australis: the role of litter. Estuaries 26(2B):475–483

    Article  Google Scholar 

  93. Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445–2449

    Article  CAS  PubMed  Google Scholar 

  94. Saltonstall K (2003a) Microsatellite variation within and among North American lineages of Phragmites australis. Mol Ecol 12:1689–1702

    Article  CAS  PubMed  Google Scholar 

  95. Saltonstall K (2003b) Genetic variation among North American populations of Phragmites australis: implications for management. Estuaries 26:444–451

    Article  Google Scholar 

  96. Saltonstall K (2003c) A rapid method for identifying the origin of North American Phragmites populations using RFLP analysis. Wetlands 23:1043–1047

    Article  Google Scholar 

  97. Saltonstall K, Stevenson JC (2007) The effect of nutrients on seedling growth of native and introduced Phragmites australis. Aquat Bot 86:331–336

    Article  CAS  Google Scholar 

  98. Saltonstall K, Peterson PM, Soreng RJ (2004) Recognition of Phragmites australis subsp. americanus (Poaceae: Arundinoideae) in North America: evidence from morphological and genetic analysis. SIDA Contrib Bot 21:683–692

    Google Scholar 

  99. Saltonstall K, Lambert A, Meyerson LA (2010) Genetics and reproduction of common (Phragmites australis) and giant reed (Arundo donax). Invasive Plant Sci Manag 3:495–505

    Article  Google Scholar 

  100. Saltonstall K, Castillo HE, Blossey B (2014) Confirmed field hybridization of native and introduced Phragmites australis (Poaceae) in North America. Am J Bot 101:211–215

    Article  PubMed  Google Scholar 

  101. Saltonstall K, Lambert AM, Rice N (2016) What happens in Vegas, better stay in Vegas: Phragmites australis hybrids in the Las Vegas Wash. Biol Invasions 18:2463–2474

    Article  Google Scholar 

  102. Schaffner U, Smith L, Cristofaro M (2018) A review of open-field host range testing to evaluate nontarget use by herbivorous biological control candidates. Biocontrol 63:405–416

    Article  Google Scholar 

  103. Simberloff D (2012) Risks of biological control for conservation purposes. Biocontrol 57:263–276

    Article  Google Scholar 

  104. Simberloff D, Stiling P (1996) How risky is biological control? Ecology 77:1965–1974

    Google Scholar 

  105. Stastny M, Sargent RD (2017) Evidence for rapid evolutionary change in an invasive plant in response to biological control. J Evol Biol 30:1042–1052

    Article  CAS  PubMed  Google Scholar 

  106. Stiling P, Cornelissen T (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biol Control 34:236–246

    Article  Google Scholar 

  107. Stohlgren TJ, Pyšek P, Kartesz J, Nishino M, Pauchard A, Winter M, Pino J, Richardson DM, Wilson JRU, Murray BR, Phillips ML, Ming-yang L, Celesti-Grapow L, Font X (2011) Widespread plant species: natives versus aliens in our changing world. Biol Invasions 13:1931–1944

    Article  Google Scholar 

  108. Stutz S, Mráz P, Hinz HL, Müller-Schärer H, Schaffner U (2018) Biological invasion of oxeye daisy (Leucanthemum vulgare) in North America: pre-adaptation, post-introduction evolution, or both? PLoS ONE 13:e0190705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Suckling DM, Sforza RFH (2014) What magnitude are observed non-target impacts from weed biocontrol? PLoS ONE 9:e84847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Swearingen J, Saltonstall K (2012) Phragmites field guide: distinguishing native and exotic forms of common reed (Phragmites australis) in the United States. Technical Note, Natural Resources Conservation Service, US Department of Agriculture

  111. Szűcs M, Schaffner U, Price WJ, Schwarzländer M (2012) Post-introduction evolution in the biological control agent Longitarsus jacobaeae (Coleoptera: Chrysomelidae). Evol Appl 5:858–868

    Article  PubMed  PubMed Central  Google Scholar 

  112. Tewksbury L, Casagrande R, Blossey B, Häfliger P, Schwarzländer M (2002) Potential for biological control of Phragmites australis in North America. Biol Control 23(2):191–212

    Article  Google Scholar 

  113. Tomasetto F, Cianciullo S, Reale M, Attorre F, Olaniyan O, Goldson SL (2018) Breakdown in classical biological control of Argentine stem weevil: a matter of time. Biocontrol 63:521–531

    Article  CAS  Google Scholar 

  114. Tulbure MG, Ghioca-Robrecht DM, Johnston CA, Whigham DF (2012) Inventory and ventilation efficiency of nonnative and native Phragmites australis (common reed) in tidal wetlands of the Chesapeake Bay. Estuaries Coasts 35:1353–1359

    Article  CAS  Google Scholar 

  115. Turner KG, Hufbauer RA, Rieseberg LH (2014) Rapid evolution of an invasive weed. New Phytol 202:309–321

    Article  PubMed  Google Scholar 

  116. USDA (U.S. Department of Agriculture) (2016) Technical advisory group for biological control agents of weeds manual. Interim edition. USDA, Washington, DC. https://www.aphis.usda.gov/import_export/plants/manuals/domestic/downloads/tag-bcaw_manual.pdf. Accessed 1 Apr 2018

  117. van Klinken RD, Edwards OR (2002) Is host specificity of weed biocontrol agents likely to evolve rapidly following establishment? Ecol Lett 5:590–595

    Article  Google Scholar 

  118. Weis JS, Weis P (2003) Is the invasion of the common reed, Phragmites australis, into tidal marshes of the eastern US an ecological disaster? Mar Pollut Bull 46(7):816–820

    Article  CAS  PubMed  Google Scholar 

  119. Whitfeld TJS, Novotny V, Miller SE, Hrcek J, Klimes P, Weiblen GD (2012) Predicting tropical insect herbivore abundance from host plant traits and phylogeny. Ecology 93:S211–S222

    Article  Google Scholar 

  120. Williams WI, Friedman JM, Gaskin JF, Norton AP (2014) Hybridization of an invasive shrub affects tolerance and resistance to defoliation by a biological control agent. Evol Appl 1:11. https://doi.org/10.1111/eva.12134

    Article  Google Scholar 

  121. Williams J, Lambert AM, Long R, Saltonstall K (2019) Does hybrid Phragmites australis differ from native and introduced lineages in reproductive, genetic, and morphological traits? Am J Bot 106:29–41

    Article  PubMed  Google Scholar 

  122. Willson KG, Perantoni AN, Berry ZC, Eicholtz MI, Tamukong YB, Yarwood SA, Baldwin AH (2017) Influences of reduced iron and magnesium on growth and photosynthetic performance of Phragmites australis subsp. americanus (North American common reed). Aquat Bot 137:30–38

    Article  CAS  Google Scholar 

  123. Windham L, Lathrop RG (1999) Effects of Phragmites australis (common reed) invasion on aboveground biomass and soil properties in brackish tidal marsh of the Mullica River, New Jersey. Estuaries 22:927–935

    Article  Google Scholar 

  124. Windham L, Weis JS, Weis P (2003) Uptake and distribution of metals in two dominant salt marsh macrophytes, Spartina alterniflora (cordgrass) and Phragmites australis (common reed). Estuar Coast Shelf Sci 56:63–72

    Article  CAS  Google Scholar 

  125. Wright MG, Bennett GM (2018) Evolution of biological control agents following introduction to new environments. Biocontrol 63:105–116

    Article  Google Scholar 

  126. Wu CA, Murray LA, Heffernan KE (2015) Evidence for natural hybridization between native and introduced lineages of Phragmites australis in the Chesapeake Bay watershed. Am J Bot 102:805–812

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Lea Stickle assisted with editing. This paper is a Hudsonia-Bard College Field Station Contribution.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Erik Kiviat.

Ethics declarations

Conflict of interest

The authors state they have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kiviat, E., Meyerson, L.A., Mozdzer, T.J. et al. Evidence does not support the targeting of cryptic invaders at the subspecies level using classical biological control: the example of Phragmites. Biol Invasions 21, 2529–2541 (2019). https://doi.org/10.1007/s10530-019-02014-9

Download citation

Keywords

  • Ecosystem services
  • Herbivory
  • Host switching
  • Invasive species
  • Non-target impacts of biocontrol
  • Phragmites australis