Advertisement

Biological Invasions

, Volume 17, Issue 12, pp 3419–3432 | Cite as

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

  • Warwick J. AllenEmail author
  • Randee E. Young
  • Ganesh P. Bhattarai
  • Jordan R. Croy
  • Adam M. Lambert
  • Laura A. Meyerson
  • James T. Cronin
Original Paper

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.

Keywords

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

Notes

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.).

Supplementary material

10530_2015_968_MOESM1_ESM.docx (134 kb)
Supplementary material 1 (DOCX 133 kb)
10530_2015_968_MOESM2_ESM.docx (60 kb)
Supplementary material 2 (DOCX 59 kb)
10530_2015_968_MOESM3_ESM.docx (31 kb)
Supplementary material 3 (DOCX 30 kb)
10530_2015_968_MOESM4_ESM.docx (33 kb)
Supplementary material 4 (DOCX 32 kb)

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 7:269–277Google Scholar
  2. Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715CrossRefGoogle 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 29:71–74CrossRefGoogle Scholar
  4. Balme G (2000) Insects on Phragmites australis. Master’s thesis. Department of Plant Sciences, University of Rhode Island, Kingston, Rhode IslandGoogle Scholar
  5. Belote RT, Weltzin JF (2006) Interactions between two co-dominant, invasive plants in the understory of a temperate deciduous forest. Biol Invasions 8:1629–1641CrossRefGoogle Scholar
  6. Bhattarai GP, Cronin JT (2014) Hurricane activity and the large-scale pattern of spread of an invasive plant species. PLoS One 9:e98478PubMedCentralCrossRefPubMedGoogle Scholar
  7. Blossey B (2003) A framework for evaluating potential ecological effects of implementing biological control of Phragmites australis. Estuaries 26:607–617CrossRefGoogle 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 110:225–230CrossRefGoogle 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 173:1397–1409CrossRefPubMedGoogle 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 13:937–946PubMedGoogle Scholar
  11. Chvala M, Doskocil J, Mook JH, Pokorny V (1974) The genus Lipara Meigen (Diptera: Chloropidae), systematics, morphology, behaviour, and ecology. Tijdschr Entomol 117:1–25Google 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 11:379–388CrossRefGoogle Scholar
  13. Clevering OA, Lissner J (1999) Taxonomy, chromosome numbers, clonal diversity and population dynamics of Phragmites australis. Aquat Bot 64:185–208CrossRefGoogle Scholar
  14. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  15. Cronin JT, Bhattarai GP, Allen WJ, Meyerson LA (2015) Biogeography of a plant invasion: plant-herbivore interactions. Ecology 96:1115–1127CrossRefPubMedGoogle Scholar
  16. Dangremond EM, Pardini EA, Knight TM (2010) Apparent competition with an invasive plant hastens the extinction of an endangered lupine. Ecology 91:2261–2271CrossRefPubMedGoogle 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 15:141–147CrossRefGoogle 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 PaulGoogle 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, OxfordGoogle Scholar
  20. De Bruyn L (1995) Plant stress and larval performance of a dipterous gall former. Oecologia 101:461–466CrossRefGoogle Scholar
  21. Desurmont GA, Donoghue MJ, Clement WL, Agrawal AA (2011) Evolutionary history predicts plant defense against an invasive pest. PNAS 108:7070–7074PubMedCentralCrossRefPubMedGoogle 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 6:511–521CrossRefGoogle Scholar
  23. Elton CS (1958) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoCrossRefGoogle 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 13:725–734CrossRefGoogle 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:e83619PubMedCentralCrossRefPubMedGoogle Scholar
  26. Funk JL, Throop HL (2009) Enemy release and plant invasion: patterns of defensive traits and leaf damage in Hawaii. Oecologia 162:815–823CrossRefPubMedGoogle 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 12:389–405CrossRefGoogle 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 92:1758–1768CrossRefPubMedGoogle 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 94:94–100CrossRefGoogle Scholar
  30. Hansen RM (1978) Shasta ground sloth food habits, Rampart Cave, Arizona. Paleobiology 4:302–319Google 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 143:2251–2259CrossRefGoogle 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 34:851–862CrossRefGoogle Scholar
  33. Hill SB, Kotanen PM (2009) Evidence that phylogenetically novel non-indigenous plants experience less herbivory. Oecologia 161:581–590CrossRefPubMedGoogle 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 10:369–379CrossRefGoogle Scholar
  35. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  36. Kulmatiski A, Beard KH, Meyerson LA, Gibson JC, Mock KE (2010) Nonnative Phragmites australis invasion into Utah wetlands. West N Am Nat 70:541–552CrossRefGoogle 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 12:3025–3031CrossRefGoogle 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 36:451–457CrossRefPubMedGoogle 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):795–799CrossRefGoogle 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 86:163–170CrossRefGoogle 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 99:538–551CrossRefPubMedGoogle Scholar
  42. Lau JA, Strauss SY (2005) Insect herbivores drive important indirect effects of exotic plants on native communities. Ecology 86:2990–2997CrossRefGoogle Scholar
  43. Levine JM, D’Antonio CM (2003) Forecasting biological invasions with increasing international trade. Conserv Biol 17:322–326CrossRefGoogle Scholar
  44. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545CrossRefGoogle 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 30:67–74CrossRefGoogle Scholar
  46. McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall, LondonCrossRefGoogle 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 13:859–867CrossRefGoogle 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 134:99–107CrossRefGoogle 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 33:413–421CrossRefGoogle 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 15:2605–2608CrossRefGoogle 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 8:89–103CrossRefGoogle 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 AngelesGoogle 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 PubMedCentralPubMedGoogle Scholar
  54. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627CrossRefPubMedGoogle Scholar
  55. Mook JH (1967) Habitat selection by Lipara lucens Mg. (Diptera, Chloropidae) and its survival value. Arch Neerlandaises Zool 17:469–549CrossRefGoogle 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:e17227PubMedCentralCrossRefPubMedGoogle 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 47:130–138CrossRefGoogle 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 PubMedCentralGoogle Scholar
  59. Nartshuk EP (1984) Family Chloropidae. In: Soos A (ed) Catalogue of Palaearctic Diptera, vol 10. Akademiai Kiado, BudapestGoogle Scholar
  60. Nartshuk EP (2006) Parasites of grass flies (Diptera, Chloropidae) from the order Hymenoptera in the Holarctic region. Entomol Rev 86:576–597CrossRefGoogle 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 3:206–214Google 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 1:149–158CrossRefGoogle Scholar
  63. Park MG, Blossey B (2008) Importance of plant traits and herbivory for invasiveness of Phragmites australis (Poaceae). Am J Bot 95:1557–1568CrossRefPubMedGoogle Scholar
  64. Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and nonnative plants. Ecology 88:1210–1224CrossRefPubMedGoogle Scholar
  65. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967CrossRefGoogle Scholar
  66. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461CrossRefPubMedGoogle 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 115:354Google Scholar
  68. Pearson DE, McKelvey KS, Ruggiero LF (2000) Non-target effects of an introduced biological control agent on deer mouse ecology. Oecologia 122:121–128CrossRefGoogle Scholar
  69. Prior KM, Hellmann JJ (2013) Does enemy loss cause release? A biogeographical comparison of parasitoid effects on an introduced insect. Ecology 94:1015–1024CrossRefGoogle Scholar
  70. R Core Team (2014) R: a language and environment for statistical computing. Version 3.0.3. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  71. Rand TA, Louda SM (2004) Exotic weed invasion increases the susceptibility of native plants to attack by a biocontrol herbivore. Ecology 85:1548–1554CrossRefGoogle Scholar
  72. Reader T (2001) Competition, kleptoparasitism and intraguild predation in a reedbed community. PhD dissertation. Darwin College, Cambridge University, UKGoogle Scholar
  73. Reader T (2003) Strong interactions between species of phytophagous fly: a case of intraguild kleptoparasitism. Oikos 103:101–112CrossRefGoogle 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 12:303–311CrossRefGoogle Scholar
  75. Sabrosky CW (1958) A Phragmites gall-maker new to North America (Diptera, Chloropidae). P Entomol Soc Wash 60:231Google Scholar
  76. Saltonstall K (2002) Cryptic invasion by a non-native genotype of Phragmites australis into North America. PNAS 99:2445–2449PubMedCentralCrossRefPubMedGoogle 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 101:211–215CrossRefPubMedGoogle 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, BozemanGoogle Scholar
  79. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32CrossRefGoogle Scholar
  80. Skuhravy V (1981) Invertebates and vertebrates attacking common reed stands (Phragmites communis) in Czechoslovakia. Czechoslovak Academy of Sciences, PragueGoogle Scholar
  81. Sopow SL, Quiring DT (2001) Is gall size a good indicator of adelgid fitness? Entomol Exp Appl 99:267–271CrossRefGoogle Scholar
  82. Stille B (1984) The effect of hostplant and parasitoids on the reproductive success of the parthenogenetic gall wasp Diplolepis rosae. Oecologia 63:364–369CrossRefGoogle Scholar
  83. Stricker KB, Stiling P (2012) Herbivory by and introduced Asian weevil negates population growth of an invasive Brazilian shrub in Florida. Ecology 93:1902–1911CrossRefPubMedGoogle 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 133:430–438CrossRefGoogle Scholar
  85. Taylor BW, Anderson CR, Peckarsky BL (1998) Effects of size at metamorphosis on stonefly fecundity, longevity, and reproductive success. Oecologia 114:494–502CrossRefGoogle 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 23:191–212CrossRefGoogle 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 PaulGoogle 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 11:279–285CrossRefPubMedGoogle 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 127:681–695CrossRefGoogle Scholar
  90. Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160:705–711CrossRefPubMedGoogle 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 27:867–872CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Warwick J. Allen
    • 1
    Email author
  • Randee E. Young
    • 1
  • Ganesh P. Bhattarai
    • 1
  • Jordan R. Croy
    • 1
  • Adam M. Lambert
    • 2
  • Laura A. Meyerson
    • 3
  • James T. Cronin
    • 1
  1. 1.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA
  2. 2.UCSB Marine Science InstituteUniversity of California at Santa BarbaraSanta BarbaraUSA
  3. 3.Natural Resources ScienceUniversity of Rhode IslandKingstonUSA

Personalised recommendations