, Volume 174, Issue 3, pp 817–826 | Cite as

Release from herbivory does not confer invasion success for Eugenia uniflora in Florida

  • Kerry Bohl Stricker
  • Peter Stiling
Plant-microbe-animal interactions - Original research


One of the most commonly cited hypotheses explaining invasion success is the enemy release hypothesis (ERH), which maintains that populations are regulated by coevolved natural enemies where they are native but are relieved of this pressure in the new range. However, the role of resident enemies in plant invasion remains unresolved. We conducted a field experiment to test predictions of the ERH empirically using a system of native, introduced invasive, and introduced non-invasive Eugenia congeners in south Florida. Such experiments are rarely undertaken but are particularly informative in tests of the ERH, as they simultaneously identify factors allowing invasive species to replace natives and traits determining why most introduced species are unsuccessful invaders. We excluded insect herbivores from seedlings of Eugenia congeners where the native and invasive Eugenia co-occur, and compared how herbivore exclusion affected foliar damage, growth, and survival. We found no evidence to support the ERH in this system, instead finding that the invasive E. uniflora sustained significantly more damage than the native and introduced species. Interestingly, E. uniflora performed better than, or as well as, its congeners in terms of growth and survival, in spite of higher damage incidence. Further, although herbivore exclusion positively influenced Eugenia seedling survival, there were few differences among species and no patterns in regard to invasion status or origin. We conclude that the ability of E. uniflora to outperform its native and introduced non-invasive congeners, and not release from insect herbivores, contributes to its success as an invader in Florida.


Enemy release hypothesis Herbivore exclusion Introduced non-invasive Phylogenetically controlled experiment Seedling performance 



We thank H. Liu and R. Pemberton for inspiring this study. We also thank R. Mapp, M. Foley, Hugh Taylor Birch State Park, P. Griffith, and Montgomery Botanical Center for providing site accommodations, Bayer CropScience for providing Merit, and H. Jezorek for field assistance. In addition, we thank Fairchild Tropical Botanic Garden, Fruit and Spice Park, the University of Florida Tropical Research and Education Center, and Plantation Heritage Park for access to plants. Finally, we would also like to acknowledge anonymous reviewers for suggestions that led to marked improvements in this manuscript. This work was supported in part by the Florida Exotic Pest Plant Council (FLEPPC) and the Fern Garden Club of Odessa. The experiments conducted comply with the current laws of the United States of America, where the experiments were performed.


  1. Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715CrossRefGoogle Scholar
  2. Ashton IW, Lerdau MT (2008) Tolerance to herbivory, and not resistance, may explain differential success of invasive, naturalized, and native North American temperate vines. Divers Distrib 14:169–178CrossRefGoogle Scholar
  3. Baskin CC, Baskin JM (1998) Seeds ecology, biogeography, and evolution of dormancy and germination. Academic Press, San DiegoGoogle Scholar
  4. Bayer Environmental Science (2004) Merit 75 WP insecticide specimen label. Bayer CropScience LP, Research Triangle ParkGoogle Scholar
  5. Bohl Stricker KR, Stiling P (2012) Herbivory by an introduced Asian weevil negatively affects population growth of an invasive Brazilian shrub in Florida. Ecology 93:1902–1911CrossRefGoogle Scholar
  6. Bohl Stricker KR, Stiling P (2013) Seedlings of the introduced invasive shrub Eugenia uniflora (Myrtaceae) outperform those of its native and introduced non-invasive congeners in Florida. Biol Invasions 15:1973–1987Google Scholar
  7. Buschmann H, Edwards PJ, Dietz H (2005) Variation in growth pattern and response to slug damage among native and invasive provenances of four perennial Brassicaceae species. J Ecol 93:322–334CrossRefGoogle Scholar
  8. Cahill JF, Kembel SW, Lamb EG, Keddy PA (2008) Does phylogenetic relatedness influence the strength of competition among vascular plants? Perspect Plant Ecol Evol Syst 10:41–50CrossRefGoogle Scholar
  9. Cappuccino N, Carpenter D (2005) Invasive exotic plants suffer less herbivory than non-invasive exotic plants. Biol Lett 1:435–438PubMedCentralPubMedCrossRefGoogle Scholar
  10. Chiriboga CA (2009) Physiological responses of woody plants to imidacloprid formulations. Master’s thesis. Ohio State University, ColumbusGoogle Scholar
  11. 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
  12. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  13. Crawley MJ (1989) Insect herbivores and plant-population dynamics. Annu Rev Entomol 34:531–564CrossRefGoogle Scholar
  14. Dawson W, Burslem D, Hulme PE (2009) Herbivory is related to taxonomic isolation, but not to invasiveness of tropical alien plants. Divers Distrib 15:141–147CrossRefGoogle Scholar
  15. DeWalt SJ (2006) Population dynamics and potential for biological control of an exotic invasive shrub in Hawaiian rainforests. Biol Invasions 8:1145–1158CrossRefGoogle Scholar
  16. DeWalt SJ, Denslow JS, Ickes K (2004) Natural-enemy release facilitates habitat expansion of the invasive tropical shrub Clidemia hirta. Ecology 85:471–483CrossRefGoogle Scholar
  17. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonCrossRefGoogle Scholar
  18. Florida Exotic Pest Plant Council (FLEPPC) (2011) FLEPPC 2011 list of invasive plant species, summer/fall 2011. Accessed 30 Jan 2013
  19. Gann GD, Bradley KA, Woodmansee SW (2007) The floristic inventory of south Florida database online. The Institute for Regional Conservation, Miami. Accessed 8 May 2007
  20. Gilman EF (2011) Eugenia axillaris. Fact sheet FPS-199. Environmental Horticulture Department, Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of FloridaGoogle Scholar
  21. Gilman EF (2011) Eugenia foetida. Fact sheet FPS-200. Environmental Horticulture Department, Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of FloridaGoogle Scholar
  22. Global Invasive Species Database (2013) Eugenia uniflora. Accessed 30 Jan 2013
  23. Gordon DR, Thomas KP (1997) Florida’s invasion by nonindigenous plants: history, screening, and regulation. In: Simberloff D, Schmitz DC, Brown TC (eds) Strangers in paradise: impact and management of nonindigenous species in Florida. Island Press, Washington, pp 21–38Google Scholar
  24. Grotkopp E, Rejmánek M (2007) High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. Am J Bot 94:526–532PubMedCrossRefGoogle Scholar
  25. Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC, Harris CJ, Licari D (2005) Life-history correlates of plant invasiveness at regional and continental scales. Ecol Lett 8:1066–1074CrossRefGoogle Scholar
  26. Hawkes CV (2007) Are invaders moving targets? The generality and persistence of advantages in size, reproduction, and enemy release in invasive plant species with time since introduction. Am Nat 170:832–843PubMedCrossRefGoogle Scholar
  27. Hendrix SD (1988) Herbivory and its impact on plant reproduction. In: Lovett Doust J, Lovett Doust L (eds) Plant reproductive ecology: patterns and strategies. Oxford University Press, New York, pp 246–263Google Scholar
  28. Hill SB, Kotanen PM (2009) Evidence that phylogenetically novel non-indigenous plants experience less herbivory. Oecologia 161:581–590PubMedCrossRefGoogle Scholar
  29. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–363CrossRefGoogle Scholar
  30. Howard RA (1989) Flora of the Lesser Antilles: leeward and windward islands, vol 5. Arnold Arboretum, Harvard University, Jamaica PlainGoogle Scholar
  31. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  32. Langeland KA, Craddock Burks K (eds) (1998) Identification and biology of non-native plants in Florida’s natural areas. University of Florida, GainesvilleGoogle Scholar
  33. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989CrossRefGoogle Scholar
  34. Lieurance D, Cipollini D (2012) Damage levels from arthropod herbivores on Lonicera maackii suggest enemy release in its introduced range. Biol Invasions 14:863–873CrossRefGoogle Scholar
  35. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545CrossRefGoogle Scholar
  36. Liu H, Stiling P, Pemberton RW, Pena J (2006) Insect herbivore faunal diversity among invasive, non-invasive and native Eugenia species: implications for the enemy release hypothesis. Fla Entomol 89:475–484CrossRefGoogle Scholar
  37. Liu H, Stiling P, Pemberton RW (2007) Does enemy release matter for invasive plants? Evidence from a comparison of insect herbivore damage among invasive, non-invasive and native congeners. Biol Invasions 9:773–781CrossRefGoogle Scholar
  38. Mack RN (1996) Predicting the identity and fate of plant invaders: emergent and emerging approaches. Biol Conserv 78Google Scholar
  39. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  40. Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373CrossRefGoogle Scholar
  41. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627PubMedCrossRefGoogle Scholar
  42. Morrison WE, Hay ME (2011) Herbivore preference for native vs. exotic plants: generalist herbivores from multiple continents prefer exotic plants that are evolutionarily naive. PLoS One 6:7CrossRefGoogle Scholar
  43. Morton J (1987) Fruits of warm climates. Julia F. Morton, MiamiGoogle Scholar
  44. Myers RL, Ewel JJ (1990) Ecosystems of Florida. University of Central Florida Press, OrlandoGoogle Scholar
  45. Parker IM (2000) Invasion dynamics of Cytisus scoparius: a matrix model approach. Ecol Appl 10:726–743CrossRefGoogle Scholar
  46. Parker IM, Gilbert GS (2007) When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology 88:1210–1224PubMedCrossRefGoogle Scholar
  47. Phillips RL (1994) Selected Eugenia species. University of Florida IFAS extension HS41. Accessed 2 Jun 2013
  48. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  49. Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do stand? In: Nentwig W (ed) Biological invasions. Springer, New York, pp 97–125Google Scholar
  50. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0Google Scholar
  51. Reichard SH, Hamilton CW (1997) Predicting invasions of woody plants introduced into North America. Conserv Biol 11:193–203CrossRefGoogle Scholar
  52. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176CrossRefGoogle Scholar
  53. Stastny M, Schaffner U, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93:27–37CrossRefGoogle Scholar
  54. Strong DR (1974) Nonasymptotic species richness models and insects of British trees. Proc Natl Acad Sci USA 71:2766–2769PubMedCrossRefGoogle Scholar
  55. Suwa T, Louda SM (2012) Combined effects of plant competition and insect herbivory hinder invasiveness of an introduced thistle. Oecologia 169:467–476PubMedCrossRefGoogle Scholar
  56. van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245PubMedCrossRefGoogle Scholar
  57. Vasquez EC, Meyer GA (2011) Relationships among leaf damage, natural enemy release, and abundance in exotic and native prairie plants. Biol Invasions 13:621–633CrossRefGoogle Scholar
  58. Vilà M, Weiner J (2004) Are invasive plant species better competitors than native plant species? Evidence from pair-wise experiments. Oikos 105:229–238CrossRefGoogle Scholar
  59. Vitousek PM, Dantonio CM, Loope LL, Rejmánek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16Google Scholar
  60. Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10Google Scholar
  61. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666CrossRefGoogle Scholar
  62. Wolfe LM (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160:705–711PubMedCrossRefGoogle Scholar
  63. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of South FloridaTampaUSA

Personalised recommendations