Biological Invasions

, Volume 14, Issue 4, pp 863–873 | Cite as

Damage levels from arthropod herbivores on Lonicera maackii suggest enemy release in its introduced range

Original Paper


The ‘enemy release hypothesis’ argues when a species is introduced to a novel habitat, release from regulation by herbivores results in increased vigor, abundance, and distribution. The invasive Asian shrub Lonicera maackii appears to benefit from an absence of arthropod herbivores in North America. We assessed the incidence, amount, and type of herbivory occurring on L. maackii in forest edge and interior habitats and investigated differences in timing of damage. In October 2008, leaves were sampled from shrubs in forest interior and edge habitat from 8 sites in Ohio. In 2009, sampling was repeated at 3 sites in spring, summer, and fall with a distinction made between long and short branches. Leaf area removed averaged 1.83% across the 8 populations in 2008 and 3.09% across the 3 populations in 2009, with forest edge plants receiving slightly more damage than forest interior plants in 2008. Additionally, long shoots received more damage than short shoots in 2009. Damage incidence was also higher in the edge habitat and on long shoots compared to short shoots. As measured in 2009, damage accumulated steadily throughout the season. Chewing was the most prevalent type of damage (76. 8%) and low level of pathogen infection was observed (4.81%). Results indicate that levels of herbivory experienced by L. maackii are relatively consistent across sites, vary slightly with habitat and branch identity, but are likely too low to impact fitness of shrubs. These findings indicate that low amounts of arthropod herbivory occur for L. maackii across its introduced range, which may contribute to its invasive success.


Herbivory Lonicera maackii Amur honeysuckle Enemy release hypothesis 



The authors thank Wright State University, the Ohio Board of Regents, and the Ohio Plant Biotechnology Consortium for funding. We thank Tom Borgman of Hamilton County Park District, Michael Enright of Five Rivers MetroParks, and Kim Landsbergen and the Franklin Park Conservatory for access to field sites and facilitation of this research. Comments by two anonymous reviewers substantially improved this manuscript.


  1. Adams JM, Fang W, Callaway RM, Cipollini D, Newell E (2009) A cross-continental test of enemy release hypothesis: leaf herbivory on Acer platanoides (L.) is three times lower in North America than in its native Europe. Biol Invasions 11:1005–1016CrossRefGoogle 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. Ballare CL (2009) Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence. Plant Cell Environ 32:713–725PubMedCrossRefGoogle Scholar
  4. Barbosa VS, Leal IR, Iannuzzi L, Almeida-Cortez J (2005) Distribution pattern of herbivorous insects in a remnant of Brazilian Atlantic forest. Neotrop Entomol 34:701–711Google Scholar
  5. Bazzaz FA (1986) Life history of colonizing plants: some demographic, genetic, and physiological features. In: Mooney H, Drake J (eds) Ecology of biological invasions of North America and Hawaii. Springer, New York, pp 96–110CrossRefGoogle Scholar
  6. Becerra JX (2003) Synchronous coadaption in an ancient case of herbivory. Proc Natl Acad Sci USA 100:12804–12807PubMedCrossRefGoogle Scholar
  7. Center TD, Dray FA (1992) Associations between water-hyacinth weevils (Neochetina eichhorniae and Neochetina bruchi) and phenological stages of Eichhornia crassipes in southern Florida. Fla Entomol 75:196–211CrossRefGoogle Scholar
  8. Chen Y, Feng X, Wang M, Jia X, Zhao Y, Dong Y (2009) Triterpene glycosides from Lonicera. II. Isolation and structural determination of glycosides from flower buds of Lonicera macranthoides. Chem Nat Compd 45:514–518CrossRefGoogle Scholar
  9. Choong MF (1996) What makes a leaf tough and how this affects the pattern of Castanopsis fissa leaf consumption by caterpillars. Funct Ecol 10:668–674CrossRefGoogle Scholar
  10. 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. saccharum L.). Biol Invasions 11:379–388CrossRefGoogle Scholar
  11. Cipollini D, Dorning M (2008) Direct and indirect effects of conditioned soils and tissue extracts of the invasive shrub, Lonicera maackii, on target plant performance. Castanea 73:166–176CrossRefGoogle Scholar
  12. Cipollini D, Stevenson R, Cipollini K (2008a) Contrasting effects of allelochemicals from two invasive plants on the performance of a nonmycorrhizal plant. Int J Plant Sci 169:371–375CrossRefGoogle Scholar
  13. Cipollini D, Stevenson R, Enright S, Eyles A, Bonello P (2008b) Phenolic metabolites in leaves of the invasive shrub, Lonicera maackii, and their potential phytotoxic and anti-herbivore effects. J Chem Ecol 34:144–152PubMedCrossRefGoogle 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. Cornelissen JHC, Werger MJA, Castro-Diez P, Van Rheenen JWA, Rowland AP (1997) Foliar nutrients in relation to growth, allocation and leaf traits in seedlings of a wide range of woody plant species and types. Oecologia 111:460–469CrossRefGoogle Scholar
  16. Cornelissen, T, Fernandes GW, Vasconcellos-Neto J (2008) Size does matter: variation in herbivory between and within plants and the plant vigor hypothesis. Oikos 117:1121–1130Google Scholar
  17. Crawley MJ (1985) Reduction of oak fecundity by low-density herbivore populations. Nature 314:163–164CrossRefGoogle Scholar
  18. Cripps MG, Schwarzlander M, McKenney JL, Hinz HL, Price WJ (2006) Biogeographical comparison of the arthropod herbivore communities associated with Lepidium draba in its native, expanded and introduced ranges. J Biogeogr 33:2107–2119CrossRefGoogle Scholar
  19. 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
  20. Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed germination of three herbs with no autotoxic effects. Plant Ecol 184:287–296CrossRefGoogle Scholar
  21. Ebeling SK, Hensen I, Auge H (2008) The invasive shrub Buddleja davidii performs better in its introduced range. Divers Distrib 14:225–233CrossRefGoogle Scholar
  22. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  23. Feng Y, Auge H, Ebeling SK (2007) Invasive Buddleja davidii allocates more nitrogen to its photosynthetic machinery than five native woody species. Oecologia 153:501–510PubMedCrossRefGoogle Scholar
  24. Flamini G, Braca A, Cioni PL, Morelli I, Tome F (1997) Three new flavonoids and other constituents from Lonicera implexa. J Nat Products 60:449–452Google Scholar
  25. Franks SJ, Kral AM, Pratt PD (2006) Herbivory by introduced insects reduces growth and survival of Melaleuca quinquenervia seedlings. Environ Entomol 35:366–372CrossRefGoogle Scholar
  26. Frenzel M, Brandl R (2003) Diversity and abundance patterns of phytophagous insect communities on alien and native host plants in the Brassicaceae. Ecography 26:723–730CrossRefGoogle Scholar
  27. Grevstad FS (2006) Ten-year impacts of the biological control agents Galerucella pusilla and G. calmariensis (coleoptera:Chrysomelidae) on purple loosestrife (Lythrum salicaria) central New York state. Biol Control 39:1–8CrossRefGoogle Scholar
  28. Guerra PC, Becerra J, Gianoli E (2010) Explaining differential herbivory in sun and shade: the case of Aristotelia chilensis saplings. Arthropod Plant Interact 4:229–235CrossRefGoogle Scholar
  29. Hartman KM, McCarthy BC (2008) Changes in forest structure and species composition following invasion by a non-indigenous shrub, amur honeysuckle (Lonicera maackii). J Torrey Bot Soc 135:245–259CrossRefGoogle Scholar
  30. Heinrich J, Svarcova I, Valentova K (2008) Lonicera caerulea: a prospective functional food and a source of biologically active compounds. Chem Listy 102:245–254Google Scholar
  31. Herms DA, Mattson WJ (1992) The dilemma of plants-to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  32. Hutchinson TF, Vankat JL (1997) Invasibility and effects of Amur honeysuckle in southwestern Ohio forests. Conserv Biol 11:1117–1124CrossRefGoogle Scholar
  33. Ishii H, Shoko A (2010) The role of crown architecture, leaf phenology and photosynthetic activity in promoting complementary use of light among coexisting species in temperate forests. Ecol Res 25:715–722CrossRefGoogle Scholar
  34. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  35. Lieurance D (2004) Leaf phenology, fecundity, and biomass allocation of the invasive shrub Lonicera maackii (rupr.) maxim in contrasting light environments. Masters thesis, Ohio UniversityGoogle Scholar
  36. Luken JO, Thieret JW (1996) Amur honeysuckle, its fall from grace. Bioscience 46:18–24CrossRefGoogle Scholar
  37. Luken JO, Tholemeier TC, Kuddes LM, Kunkel BA (1995a) Performance, plasticity, and acclimation of the nonindigenous shrub Lonicera maackii (Caprifoliaceae) in contrasting light environments. Can J Bot 73:1953–1961CrossRefGoogle Scholar
  38. Luken JO, Tholemeier TC, Kunkel BA, Kuddes LM (1995b) Branch architecture plasticity of amur honeysuckle (Lonicera-maackii (rupr) herder)—initial response in extreme light environments. J Torrey Bot Soc 122:190–195CrossRefGoogle Scholar
  39. Luken JO, Kuddes LM, Tholemeier TC (1997a) Response of understory species to gap formation and soil disturbance in Lonicera maackii thickets. Restor Ecol 5:229–235CrossRefGoogle Scholar
  40. Luken JO, Kuddes LM, Tholemeier TC, Haller DM (1997b) Comparative responses of Lonicera maackii (amur honeysuckle) and Lindera benzoin (spicebush) to increased light. Am Midl Nat 138:331–343CrossRefGoogle Scholar
  41. Machida K, Sasaki H, Iijima T, Kikuchi M (2002) Studies on the constituents of Lonicera species. XVII. New iridoid glycosides of the stems and leaves of Lonicera japonica THUNB. Chem Pharm Bull 50:1041–1044PubMedCrossRefGoogle Scholar
  42. Matlack GR (1993) Microenvironmental variation within and among forest edge sites in the eastern United States. Biol Conserv 66:185–194CrossRefGoogle Scholar
  43. McEwan RW, Rieske LK, Arthur MA (2009a) Potential interactions between invasive woody shrubs and the gypsy moth (Lymantria dispar), an invasive insect herbivore. Biol Invasions 11:1053–1058CrossRefGoogle Scholar
  44. McEwan RW, Birchfield MK, Schoergendorfer A, Arthur MA (2009b) Leaf phenology and freeze tolerance of the invasive shrub amur honeysuckle and potential native competitors. J Torrey Bot Soc 136:212–220CrossRefGoogle Scholar
  45. Medley KE (1997) Distribution of the non-native shrub Lonicera maackii in Kramer woods, Ohio. Phys Geogr 18:18–36Google Scholar
  46. Morrison JA, Mauck K (2007) Experimental field comparison of native and non-native maple seedlings: natural enemies, ecophysiology, growth and survival. J Ecol 95:1036–1049CrossRefGoogle Scholar
  47. Ochmian I, Oszmianski J, Skupien K (2009) Chemical composition, phenolics, and firmness of small black fruits. J Appl Bot Food Qual 83:64–69Google Scholar
  48. Osunkoya OO, Bayliss D, Panetta FD, Vivian-Smith G (2010a) Variation in ecophysiology and carbon economy of invasive and native woody vines of riparian zones in south-eastern Queensland. Austral Ecol 35:636–649CrossRefGoogle Scholar
  49. Osunkoya OO, Bayliss D, Panetta FD, Vivian-Smith G (2010b) Leaf trait co-ordination in relation to construction cost, carbon gain and resource-use efficiency in exotic invasive and native woody vine species. Ann Bot 106:371–380PubMedCrossRefGoogle Scholar
  50. Ozanne CMP, Speight MR, Hambler C, Evans HF (2000) Isolated trees and forest patches: patterns in canopy arthropod abundance and diversity in Pinus sylvestrus (Scots Pine). For Ecol Manage 137:53–63CrossRefGoogle Scholar
  51. Pennington DN, Hansel JR, Gorchov DL (2010) Urbanization and riparian forest woody communities: diversity, composition, and structure within a metropolitan landscape. Biol Conserv 143:182–194CrossRefGoogle Scholar
  52. Penuelas J, Sardans J, Stefanescu C, Parella T, Filella I (2006) Lonicera implexa leaves bearing naturally laid eggs of the specialist herbivore Euphydryas aurinia have dramatically greater concentrations of iridoid glycosides than other leaves. J Chem Ecol 32:1925–1933PubMedCrossRefGoogle Scholar
  53. Poorter L, de Plassche MV, Willems S, Boot RGA (2004) Leaf traits and herbivory rates of tropical tree species differing in successional status. Plant Biol 6:746–754PubMedCrossRefGoogle Scholar
  54. Price PW (1991) Plant vigor hypothesis and herbivore attack. Oikos 62:244–251CrossRefGoogle Scholar
  55. Ren M, Chen J, Song Y, Sheng L, Li P, Qi L (2008) Identification and quantification of 32 bioactive compounds in Lonicera species by high performance liquid chromatography coupled with time-of-flight mass spectrometry. J Pharm Biomed Anal 48:1351–1360PubMedCrossRefGoogle Scholar
  56. Ries L, Fletcher RJ, Battin J, Sisk TD (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu Rev Ecol Evol Syst 35:491–522CrossRefGoogle Scholar
  57. Schierenbeck KA, Marshall JD (1993) Seasonal and diurnal patterns of photosynthetic gas-exchange for Lonicera sempervirens and L. japonica (Caprifoliaceae). Am J Bot 80:1292–1299Google Scholar
  58. Schierenbeck KA, Mack RN, Sharitz RR (1994) Effects of herbivory on growth and biomass allocation in native and introduced species of Lonicera. Ecology 75:1661–1672CrossRefGoogle Scholar
  59. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185PubMedCrossRefGoogle Scholar
  60. Trisel DE (1997) The invasive shrub Lonicera maackii (Rupr.) Herder (Caprifoliaceae); factors contributing to its success and its effect on native species. Dissertation, Miami UniversityGoogle Scholar
  61. Waipara NW, Winks CJ, Smith LA, Wilke JP (2007) Natural enemies of Japanese honeysuckle Lonicera japonica, in New Zealand. NZ Plant Prot 60:158–163Google Scholar
  62. Watling JI, Orrock JL (2010) Measuring edge contrast using biotic criteria helps define edge effects on the density of an invasive plant. Landsc Ecol 25:69–78CrossRefGoogle Scholar
  63. Whittaker JB, Warrington S (1985) An experimental field study of different levels of insect herbivory induced by Formica rufa predation on sycamore (Acer pseudoplatanus) III. Effects on tree growth. J Appl Ecol 22:797–811CrossRefGoogle Scholar
  64. Zheng H, Wu Y, Ding J, Binion D, Fu W, Reardon R (2006) Invasive plants established in the United States that are found in Asia and their associated natural enemies vol 1. General Technical Report Number FHTET 2005-15. Chinese Academy of Sciences, Beijing, ChinaGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Biological Sciences and Environmental Sciences PhD ProgramWright State UniversityDaytonUSA

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