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Multitrophic enemy escape of invasive Phragmites australis and its introduced herbivores in North America

Abstract

One explanation for why invasive species are successful is that they escape natural enemies from their native range or experience lower attack from natural enemies in the introduced range relative to native species (i.e., the enemy-release hypothesis). However, little is known about how invasive plants interact with co-introduced herbivores or natural enemies of the introduced herbivores. We focus on Phragmites australis, a wetland grass native to Europe (EU) and North America (NA). Within the past 100–150 years, invasive European genotypes of P. australis and several species of specialist Lipara gall flies have spread within NA. On both continents we surveyed P. australis patches for Lipara infestation (proportion of stems infested) and Lipara mortality from natural enemies. Our objectives were to assess evidence for enemy-release in the invaded (NA) versus native (EU) range and whether Lipara infestation or mortality differed between invasive and native P. australis genotypes in NA. Enemy-release varied regionally; Lipara were absent throughout most of NA, supporting enemy-release of Phragmites. However, where Lipara were present, the proportion of invasive P. australis stems infested with Lipara was higher in the introduced (11 %) than native range (<1 %). This difference may be explained by the absence of Lipara parasitoids in our NA survey, strongly supporting enemy-release of Lipara. In NA, native P. australis genotypes exhibited higher Lipara infestation (32 %) than invasive genotypes (11 %), largely driven by L. rufitarsis. We attribute genotypic differences in infestation to a combination of Lipara exhibiting 34 % greater performance (gall diameter) and suffering four times less vertebrate predation on native than invasive genotypes. Our study suggests that complex interactions can result from the co-introduction of plants and their herbivores, and that a multitrophic perspective is required for investigating how biotic interactions influence invasion success.

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References

  1. Abraham R, Carstensen B (1982) Die schilfgallen von Lipara-arten (Diptera: Chloropidae) und ihre bewohner im schilf der Haseldorfer Marsch bei Hamburg. Entomol Mitt Zool Mus Hambg Bd 7:269–277

    Google Scholar 

  2. Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715

    Article  Google Scholar 

  3. Athen O, Tsharntke T (1999) Insect communities of Phragmites habitat used for sewage purification: effect of age and area of habitats on species richness and herbivore-parasitoid interaction. Limnologica 29:71–74

    Article  Google Scholar 

  4. Balme G (2000) Insects on Phragmites australis. Master’s thesis. Department of Plant Sciences, University of Rhode Island, Kingston, Rhode Island

  5. Belote RT, Weltzin JF (2006) Interactions between two co-dominant, invasive plants in the understory of a temperate deciduous forest. Biol Invasions 8:1629–1641

    Article  Google Scholar 

  6. Bhattarai GP, Cronin JT (2014) Hurricane activity and the large-scale pattern of spread of an invasive plant species. PLoS One 9:e98478

    PubMed Central  Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  8. Brisson J, Paradis E, Bellavance M (2008) Evidence of sexual reproduction in the invasive common reed (Phragmites australis subsp. australis; Poaceae) in Eastern Canada: a possible consequence of global warming? Rhodora 110:225–230

    Article  Google Scholar 

  9. Castells E, Morante M, Blanco-Moreno JM, Sans FX, Vilatersana R, Blasco-Moreno A (2013) Reduced seed predation after invasion supports enemy release in a broad biogeographical survey. Oecologia 173:1397–1409

    Article  PubMed  Google Scholar 

  10. Chun YJ, van Kleunen M, Dawson W (2010) The role of enemy release, tolerance and resistance in plant invasions: linking damage to performance. Ecol Lett 13:937–946

    PubMed  Google Scholar 

  11. Chvala M, Doskocil J, Mook JH, Pokorny V (1974) The genus Lipara Meigen (Diptera: Chloropidae), systematics, morphology, behaviour, and ecology. Tijdschr Entomol 117:1–25

    Google Scholar 

  12. Cincotta CL, Adams JM, Holzapfel C (2009) Testing the enemy release hypothesis: a comparison of foliar insect herbivory of the exotic Norway maple (Acer platanoides L.) and the native sugar maple (A. sacharum L.). Biol Invasions 11:379–388

    Article  Google Scholar 

  13. Clevering OA, Lissner J (1999) Taxonomy, chromosome numbers, clonal diversity and population dynamics of Phragmites australis. Aquat Bot 64:185–208

    Article  Google Scholar 

  14. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  15. 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 

  16. Dangremond EM, Pardini EA, Knight TM (2010) Apparent competition with an invasive plant hastens the extinction of an endangered lupine. Ecology 91:2261–2271

    Article  PubMed  Google Scholar 

  17. Dawson W, Burslem DFRP, Hulme PE (2009) Herbivory is related to taxonomic isolation, but not to invasiveness of tropical alien plants. Divers Distrib 15:141–147

    Article  Google Scholar 

  18. De Bruyn L (1993) Life history strategies of three gall-forming flies tied to natural variation in growth of Phragmites australis. In: Price PW, Mattson WJ, Baranchikov YN (eds) The ecology and evolution of gall-forming insects. United States Department of Agriculture Forest Service, Saint Paul

    Google Scholar 

  19. De Bruyn L (1994) Life cycle strategies in a guild of dipteran gall formers on the common reed. In: Williams M (ed) Plant-galls: organisms, interactions, populations. Clarendon Press, Oxford

    Google Scholar 

  20. De Bruyn L (1995) Plant stress and larval performance of a dipterous gall former. Oecologia 101:461–466

    Article  Google Scholar 

  21. Desurmont GA, Donoghue MJ, Clement WL, Agrawal AA (2011) Evolutionary history predicts plant defense against an invasive pest. PNAS 108:7070–7074

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  22. Dietz H, Wirth LR, Buschmann H (2004) Variation in herbivore damage to invasive and native woody plant species in open forest vegetation on Mahé, Seychelles. Biol Invasions 6:511–521

    Article  Google Scholar 

  23. Elton CS (1958) The ecology of invasions by animals and plants. University of Chicago Press, Chicago

    Book  Google Scholar 

  24. Engelkes T, Wouters B, Bezemer TM, Harvey JA, van der Putten WH (2012) Contrasting patterns of herbivore and predator pressure on invasive and native plants. Basic Appl Ecol 13:725–734

    Article  Google Scholar 

  25. Fan S, Yu D, Liu C (2013) The invasive plant Alternanthera philoxeroides was suppressed more intensively than its native congener by a native generalist: implications for the biotic resistance hypothesis. PLoS One 8:e83619

    PubMed Central  Article  PubMed  Google Scholar 

  26. Funk JL, Throop HL (2009) Enemy release and plant invasion: patterns of defensive traits and leaf damage in Hawaii. Oecologia 162:815–823

    Article  PubMed  Google Scholar 

  27. Gandhi KJK, Herms DA (2009) Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol Invasions 12:389–405

    Article  Google Scholar 

  28. Green PT, O’Dowd DJ, Abbott KL, Jeffery M, Retallick K, MacNally R (2011) Invasional meltdown: invader-invader mutualism facilitates a secondary invasion. Ecology 92:1758–1768

    Article  PubMed  Google Scholar 

  29. Grochowska M (2013) Morphology of preimaginal stages of Lipara lucens (Diptera, Chloropidae)—a gall-forming fly in the common reed (Phragmites australis). Acta Zool 94:94–100

    Article  Google Scholar 

  30. Hansen RM (1978) Shasta ground sloth food habits, Rampart Cave, Arizona. Paleobiology 4:302–319

    Google Scholar 

  31. Harvey JA, Bukovinszky T, van der Putten WH (2010) Interactions between invasive plants and insect herbivores: a plea for a multitrophic perspective. Biol Conserv 143:2251–2259

    Article  Google Scholar 

  32. Hauber DP, Saltonstall K, White DA, Hood CS (2011) Genetic variation in the common reed, Phragmites australis, in the Mississippi River Delta marshes: evidence for multiple introductions. Estuar Coast 34:851–862

    CAS  Article  Google Scholar 

  33. Hill SB, Kotanen PM (2009) Evidence that phylogenetically novel non-indigenous plants experience less herbivory. Oecologia 161:581–590

    Article  PubMed  Google Scholar 

  34. Howard R, Travis JSE, Stiles BA (2008) Rapid growth of a Eurasian genotype of Phragmites australis in a restored brackish marsh in Louisiana, USA. Biol Invasions 10:369–379

    Article  Google Scholar 

  35. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  36. Kulmatiski A, Beard KH, Meyerson LA, Gibson JC, Mock KE (2010) Nonnative Phragmites australis invasion into Utah wetlands. West N Am Nat 70:541–552

    Article  Google Scholar 

  37. La Pierre KJ, Harpole WS, Suding KN (2010) Strong feeding preference of an exotic generalist herbivore for an exotic forb: a case of invasional antagonism. Biol Invasions 12:3025–3031

    Article  Google Scholar 

  38. 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 

  39. Lambert AM, Dudley TL (2014) Exotic wildland weeds serve as reservoirs for a newly introduced cole crop pest, Bagrada hilaris (Hemiptera: Pentatomidae). J Appl Entomol 138(10):795–799

    Article  Google Scholar 

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

    Article  Google Scholar 

  41. Lambertini C, Mendelsshon I, Gustafsson MGH, 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

    CAS  Article  PubMed  Google Scholar 

  42. Lau JA, Strauss SY (2005) Insect herbivores drive important indirect effects of exotic plants on native communities. Ecology 86:2990–2997

    Article  Google Scholar 

  43. Levine JM, D’Antonio CM (2003) Forecasting biological invasions with increasing international trade. Conserv Biol 17:322–326

    Article  Google Scholar 

  44. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545

    Article  Google Scholar 

  45. McCormick MK, Kettenring KM, Baron HM, Whigham DF (2010) Extent and reproductive mechanisms of Phragmites australis spread in brackish wetlands in Chesapeake Bay, Maryland (USA). Wetlands 30:67–74

    Article  Google Scholar 

  46. McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall, London

    Book  Google Scholar 

  47. McKinnon ML, Quiring DT, Bauce E (1999) Influence of tree growth rate, shoot size and foliar chemistry on the abundance and performance of a galling adelgid. Funct Ecol 13:859–867

    Article  Google Scholar 

  48. Meadows RE, Saltonstall K (2007) Distribution of native and introduced Phragmites australis in freshwater and oligohaline tidal marshes of the Delmarva Peninsula and southern New Jersey. J Torrey Bot Soc 134:99–107

    Article  Google Scholar 

  49. Menéndez R, González-Megías A, Lewis OT, Shaw MR, Thomas CD (2008) Escape from natural enemies during climate-driven range expansion: a case study. Ecol Entomol 33:413–421

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  52. 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) Human impacts on salt marshes: a global perspective. University of California Press, Los Angeles

    Google Scholar 

  53. Meyerson LA, Lambertini C, McCormick MK, Whigham DF (2012) Hybridization of common reed in North America? The answer is blowing in the wind. AoB Plants. doi:10.1093/aobpla/pls022

    PubMed Central  PubMed  Google Scholar 

  54. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    CAS  Article  PubMed  Google Scholar 

  55. Mook JH (1967) Habitat selection by Lipara lucens Mg. (Diptera, Chloropidae) and its survival value. Arch Neerlandaises Zool 17:469–549

    Article  Google Scholar 

  56. Morrison WE, Hay ME (2011) Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naïve. PLoS One 6:e17227

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  57. Morrison EB, Lindell CA, Holl KD, Zahawi RA (2010) Patch size effects on avian foraging behavior: implications for tropical forest restoration design. J Appl Ecol 47:130–138

    Article  Google Scholar 

  58. Mozdzer TJ, Brisson J, Hazelton ELG (2013) Physiological ecology and functional traits of North America native and Eurasian introduced Phragmites australis lineages. AOB Plants. doi:10.1093/aobpla/plt048

    PubMed Central  Google Scholar 

  59. Nartshuk EP (1984) Family Chloropidae. In: Soos A (ed) Catalogue of Palaearctic Diptera, vol 10. Akademiai Kiado, Budapest

    Google Scholar 

  60. Nartshuk EP (2006) Parasites of grass flies (Diptera, Chloropidae) from the order Hymenoptera in the Holarctic region. Entomol Rev 86:576–597

    Article  Google Scholar 

  61. Nartshuk EP (2007) Gall forming Lipara Meigen (Diptera: Chloropidae) on reed (Phragmites australis) and their inquilines and parasites in the eastern European plains. Povolz Ecol J 3:206–214

    Google Scholar 

  62. Orson RA (1999) A paleoecological assessment of Phragmites australis in New England tidal marshes: changes in plant community structure during the last few millennia. Biol Invasions 1:149–158

    Article  Google Scholar 

  63. 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 

  64. Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and nonnative plants. Ecology 88:1210–1224

    Article  PubMed  Google Scholar 

  65. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967

    Article  Google Scholar 

  66. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461

    CAS  Article  PubMed  Google Scholar 

  67. Pearson DE, Ortega YK (2002) Evidence of an indirect dispersal pathway for spotted knapweed, Centaurea maculosa, seeds, via deer mice, Peromyscus maniculatus, and great horned owls, Bubo virginianus. Can Field Nat 115:354

    Google Scholar 

  68. Pearson DE, McKelvey KS, Ruggiero LF (2000) Non-target effects of an introduced biological control agent on deer mouse ecology. Oecologia 122:121–128

    Article  Google Scholar 

  69. Prior KM, Hellmann JJ (2013) Does enemy loss cause release? A biogeographical comparison of parasitoid effects on an introduced insect. Ecology 94:1015–1024

    Article  Google Scholar 

  70. R Core Team (2014) R: a language and environment for statistical computing. Version 3.0.3. R Foundation for Statistical Computing, Vienna, Austria

  71. Rand TA, Louda SM (2004) Exotic weed invasion increases the susceptibility of native plants to attack by a biocontrol herbivore. Ecology 85:1548–1554

    Article  Google Scholar 

  72. Reader T (2001) Competition, kleptoparasitism and intraguild predation in a reedbed community. PhD dissertation. Darwin College, Cambridge University, UK

  73. Reader T (2003) Strong interactions between species of phytophagous fly: a case of intraguild kleptoparasitism. Oikos 103:101–112

    Article  Google Scholar 

  74. Relva MA, Nuñez MA, Simberloff D (2010) Introduced deer reduce native plant cover and facilitate invasion of non-native tree species: evidence for invasional meltdown. Biol Invasions 12:303–311

    Article  Google Scholar 

  75. Sabrosky CW (1958) A Phragmites gall-maker new to North America (Diptera, Chloropidae). P Entomol Soc Wash 60:231

    Google Scholar 

  76. Saltonstall K (2002) Cryptic invasion by a non-native genotype of Phragmites australis into North America. PNAS 99:2445–2449

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  77. 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 

  78. Schwarzlander M, Hafliger P (2000) Shoot flies, gall midges, and shoot and rhizome mining moths associated with common reed in Europe and their potential for biological control. In: Spencer NR (ed) Proceedings of the 10th international symposium on biological control of weeds. Montana State University, Bozeman

    Google Scholar 

  79. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32

    Article  Google Scholar 

  80. Skuhravy V (1981) Invertebates and vertebrates attacking common reed stands (Phragmites communis) in Czechoslovakia. Czechoslovak Academy of Sciences, Prague

    Google Scholar 

  81. Sopow SL, Quiring DT (2001) Is gall size a good indicator of adelgid fitness? Entomol Exp Appl 99:267–271

    Article  Google Scholar 

  82. Stille B (1984) The effect of hostplant and parasitoids on the reproductive success of the parthenogenetic gall wasp Diplolepis rosae. Oecologia 63:364–369

    Article  Google Scholar 

  83. Stricker KB, Stiling P (2012) Herbivory by and introduced Asian weevil negates population growth of an invasive Brazilian shrub in Florida. Ecology 93:1902–1911

    Article  PubMed  Google Scholar 

  84. Tammaru T, Esperk T, Castellanos I (2002) No evidence for costs of being large in females of Orgyia spp. (Lepidoptera, Lymantriidae): larger is always better. Oecologia 133:430–438

    Article  Google Scholar 

  85. Taylor BW, Anderson CR, Peckarsky BL (1998) Effects of size at metamorphosis on stonefly fecundity, longevity, and reproductive success. Oecologia 114:494–502

    Article  Google Scholar 

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

    Article  Google Scholar 

  87. Tscharntke T (1994) Tritrophic interactions in gallmaker communities on Phragmites australis: testing ecological hypotheses. In: Price PW, Mattson WJ, Baranchikov YN (eds) The ecology and evolution of gall-forming insects. United States Department of Agriculture Forest Service, Saint Paul

    Google Scholar 

  88. Vachon N, Freeland JR (2011) Phylogeographic inferences from chloroplast DNA: quantifying the effects of mutations in repetitive and non-repetitive sequences. Mol Ecol Resour 11:279–285

    CAS  Article  PubMed  Google Scholar 

  89. Weis AE, Abrahamson WG (1986) Evolution of the host-plant manipulation by gall makers: ecological and genetic factors in the Solidago-Eurosta system. Am Nat 127:681–695

    Article  Google Scholar 

  90. Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160:705–711

    Article  PubMed  Google Scholar 

  91. Zheng YL, Feng YL, Wang RF, Shi XD, Lei YB, Han LH (2012) Invasive Eupatorium adenophorum suffers lower enemy impact on carbon assimilation than native congeners. Ecol Res 27:867–872

    Article  Google Scholar 

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Acknowledgments

Thanks to the stakeholders and landowners who allowed us access: Rachel Carson National Wildlife Refuge, Choptank Nature Conservancy, Palm Beach County Parks Department, Rockefeller Wildlife Refuge, Alice Welford, Mackay Island National Wildlife Refuge, Pettipaug Yacht Club, Sheepscot Valley Conservation Association, and Estell Manor State Park. Thanks also to B. Elderd, R. Andrews, A. Chow, A. Hunt, A. Flora, J. Maynard, H. Baldwin, D. Cummings, J. Anderson, M. Burger, C. Meyerson, M. Meyerson, F. Meyerson, C. Lambertini, and H. Brix for lab and field assistance. We also thank C. Rohal, E. Hazelton, and T. Reader for useful discussion, and the two anonymous reviewers for their comments which improved the quality of this manuscript. This project was funded by NSF grant numbers DEB 1050084 (to J.T.C.) and 1049914 (to L.A.M.), the Louisiana Environmental Education Commission (to W.J.A.), and the University of Rhode Island Agricultural Experiment Station grant number RI00H-332, 311000-6044 (to L.A.M.).

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Allen, W.J., Young, R.E., Bhattarai, G.P. et al. Multitrophic enemy escape of invasive Phragmites australis and its introduced herbivores in North America. Biol Invasions 17, 3419–3432 (2015). https://doi.org/10.1007/s10530-015-0968-2

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Keywords

  • Biotic resistance
  • Chloropidae
  • Enemy release
  • Invasive plants
  • Invasional meltdown
  • Lipara spp. natural enemies