, Volume 172, Issue 4, pp 1203–1212 | Cite as

Enemy release promotes range expansion in a host plant

  • Poppy Lakeman-Fraser
  • Robert M. Ewers
Global change ecology - Original research


Climate is considered to be the predominant driver shaping species distributions at macroecological scales, yet the importance of incorporating biotic interactions in predicting future range margins under climate change scenarios is increasingly being recognised. We used translocation studies to investigate how survival and growth patterns of an understory shrub planted at latitudes within its range, at its range limit and beyond its polewards boundary (in areas it may colonise as a result of shifting climate envelopes) are affected by the presence of a primary herbivore. Specifically, we tested the null hypotheses that: (1) biotic interactions do not exert a significant role in limiting survival and growth rates across the limits of a host plant’s latitudinal range, and (2) at smaller spatial scales biotic interactions do not exert a significant role in determining survival and growth rates at edge versus interior position within a forest fragment. We found that the understory shrub Macropiper excelsum is able to survive polewards of its current latitudinal limit within the first year after transplant; in fact, growth is higher outside the plant’s current natural range than within its present-day distribution. This trend is particularly pronounced in forest core environments and corresponds closely to patterns of reduced herbivory outside the plant’s range. The absence of the primary herbivore, Cleora scriptaria, and concomitant reduction in the suppressive effects of herbivory outside of the plant’s range appear to be supporting enhanced growth and survival. If host plants are able to successfully track their climatic niche and disperse into novel areas prior to the arrival of their natural predators, it is possible that ‘enemy release’ may facilitate the establishment of plant species. These findings highlight the importance of considering biotic interactions alongside abiotic variables when predicting future species’ ranges under climate change.


Biotic interactions Climate change Predator release Range margin Translocation 



We would like to acknowledge the Grantham Institute for Climate Change and the Gilchrist Educational Trust for funding this research. Thanks go to the University of Canterbury for providing glasshouse facilities and vehicle use and to Dave Conder for his assistance in cultivating experimental plants. For access to experimental plots we thank the Dunedin, Timaru, Christchurch and Nelson Councils, DOC and private land owners Hugh Wilson, Sonia and Mark Armstrong. Graham Banton and Ben Rodriguez were instrumental in assisting with the experimental set up and data collection in New Zealand. The experiments comply with the current laws of New Zealand where the experiments were performed.


  1. Araujo MB, Guisan A (2006) Five (or so) challenges for species distribution modelling. J Biogeogr 33:1677–1688CrossRefGoogle Scholar
  2. Araújo MB, Luoto M (2007) The importance of biotic interactions for modelling species distributions under climate change. Glob Ecol Biogeogr 16:743–753CrossRefGoogle Scholar
  3. Beaugrand G, Reid PC, Ibañez F, Lindley JA, Edwards M (2002) Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296:1692–1694CrossRefPubMedGoogle Scholar
  4. Box EO (1981) Macroclimate and plant forms: an introduction to predictive modelling in phytogeography. Junk, The HagueCrossRefGoogle Scholar
  5. Brooker RW, Travis JMJ, Clark EJ, Dytham C (2007) Modelling species’ range shifts in a changing climate: the impacts of biotic interactions, dispersal distance and the rate of climate change. J Theor Biol 245:59–65CrossRefPubMedGoogle Scholar
  6. Bullock JM, Edwards RJ, Carey PD, Rose RJ (2000) Geographical separation of two Ulex species at three spatial scales: does competition limit species’ ranges? Ecography 23:257–271CrossRefGoogle Scholar
  7. Chen I-C, Hill JK, Ohlemuller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026CrossRefPubMedGoogle Scholar
  8. Clausen JD, Keck D, Hiesey WM (1940) Experimental studies on the nature of species. I. Effect of varied environments on western North American plants. Washington, DCGoogle Scholar
  9. Connell JH (2011) The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecol Soc Am 42:710–723Google Scholar
  10. Davies-Colley RJ, Payne GW, van Elswijk M, Elswijk MV (2000) Microclimate gradients across a forest edge. N Z J Ecol 24:111–121Google Scholar
  11. Davis MB, Shaw RG (2001) Range shifts and adaptive responses to Quaternary climate change. Science 292:673–679CrossRefPubMedGoogle Scholar
  12. Davis AJ, Lawton JH, Shorrocks B, Jenkinson LS (1998) Individualistic species responses invalidate simple physiological models of community dynamics under global environmental change. J Anim Ecol 67:600–612CrossRefGoogle Scholar
  13. DeFrenne P, Kolb A, Verheyen K, Brunet J, Chabrerie O, Decocq G, Diekmann M, Eriksson O, Heinken T, Hermy M, Jogar U, Stanton S, Quataert P, Zindel R, Zobel M, Graae BJ, Jõgar Ü (2009) Unravelling the effects of temperature, latitude and local environment on the reproduction of forest herbs. Glob Ecol Biogeogr 18:641–651CrossRefGoogle Scholar
  14. DeRivera CE, Ruiz GM, Hines AH, Jivoff P, Derivera CE (2005) Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86:3364–3376CrossRefGoogle Scholar
  15. Elith J, Leathwick JR (2009) Species distribution models: ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697CrossRefGoogle Scholar
  16. Ewers RM, Kliskey AD, Walker S, Rutledge D, Harding JS, Didham RK (2006) Past and future trajectories of forest loss in New Zealand. Biol Conserv 133:312–325CrossRefGoogle Scholar
  17. Gardner RO (1997) Macropiper (Piperaceae) in the south-west Pacific. N Z J Bot 35:293–307CrossRefGoogle Scholar
  18. Gaston JK (2003) The structure and dynamics of geographic ranges. Oxford University Press, USAGoogle Scholar
  19. Grashof-Bokdam CJ, Geertsema W (1998) The effect of isolation and history on colonization patterns of plant species in secondary woodland. J Biogeogr 25:837–846CrossRefGoogle Scholar
  20. Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009CrossRefGoogle Scholar
  21. Hampe A (2004) Bioclimate envelope models: what they detect and what they hide. Glob Ecol Biogeogr 13:469–471CrossRefGoogle Scholar
  22. Heikkinen RK, Luoto M, Virkkala R, Pearson RG, Körber J-H, Korber J (2007) Biotic interactions improve prediction of boreal bird distributions at macro-scales. Glob Ecol Biogeogr 16:754–763CrossRefGoogle Scholar
  23. Hickling R, Roy DB, Hill JK, Fox R, Thomas CD (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Glob Change Biol 12:450–455CrossRefGoogle Scholar
  24. Hodge S (1998) Herbivore damage and leaf loss in the New Zealand pepper tree (’Kawakawa’; Macopiper excelsum; Piperaceae). N Z J Ecol 22:173–180Google Scholar
  25. Holdridge LR (1947) Determination of world plant formations from simple climatic data. Science 105:367–368CrossRefPubMedGoogle Scholar
  26. Ibáñez I, Clark JS, Dietze MC (2008) Evaluating the sources of potential migrant species: implications under climate change. Ecol Appl 18:1664–1678CrossRefPubMedGoogle Scholar
  27. Ibáñez I, Silander JA Jr, Allen JM, Treanor S, Wilson A (2009a) Identifying hotspots for plant invasions and forecasting focal points of further spread. J Appl Ecol 46:1219–1228CrossRefGoogle Scholar
  28. Ibáñez I, Silander JA Jr, Wilson AM, LaFleur N, Tanaka N, Tsuyama I (2009b) Multivariate forecasts of potential distributions of invasive plant species. Ecol Appl 19:359–375CrossRefPubMedGoogle Scholar
  29. IPCC (2007) Climate change synthesis report. In: Pachauri RK, Reisinger A (eds) Contribution of Working Groups I, II and III to the Fourth Assessment report of the Intergovernmental Panel on Climate ChangeGoogle Scholar
  30. Jiménez-Valverde A, Lobo JM, Hortal J (2008) Not as good as they seem: the importance of concepts in species distribution modelling. Divers Distrib 14:885–890CrossRefGoogle Scholar
  31. Kawecki TJ (2008) Adaptation to marginal habitats. Annu Rev Ecol Evol Syst 39:321–342CrossRefGoogle Scholar
  32. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  33. Kollmann J, Bañuelos MJ, Banuelos MJ (2004) Latitudinal trends in growth and phenology of the invasive alien plant Impatiens glandulifera (Balsaminaceae). Divers Distrib 10:377–385CrossRefGoogle Scholar
  34. Lapointe BE, Pierce F, William B, Burnett B, Grant S (2011) Nutrient thresholds for bottom-up control of macroalgal Jamaica and southeast Florida. Limnol Oceanogr 42:1119–1131CrossRefGoogle Scholar
  35. Leathwick J, McGlone M, Walker S (2004) New Zealand’s potential vegetation pattern. Whenua, LincolnGoogle Scholar
  36. Macel M, Lawson CS, Mortimer SR, Šmilauerova M, Crémieux L, Doležal J, Edwards AR, Lanta V, Martijn T, Putten WHVD, Igual JM, Rodriguez-barrueco C, Müller- H, Steinger T, Lawson S, Edwards R, Dolezal J (2007) Climate versus soil factors in local adaptation of two common plant species. Ecology 88:424–433CrossRefPubMedGoogle Scholar
  37. Magnani F (2009) Phenotypic variability: underlying mechanisms and limits do matter. New Phytol 184:277–279CrossRefPubMedGoogle Scholar
  38. Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373CrossRefGoogle Scholar
  39. Marsico TD, Hellmann JJ (2009) Dispersal limitation inferred from an experimental translocation of Lomatium (Apiaceae) species outside their geographic ranges. Oikos 118:1783–1792CrossRefGoogle Scholar
  40. Matesanz S, Gianoli E, Valladares F (2010) Global change and the evolution of phenotypic plasticity in plants. In: Schlichting CD, Mousseau TA (eds) Year in evolutionary biology. Wiley-Blackwell, Malden, pp 35–55Google Scholar
  41. Meier ES, Kienast F, Pearman PB, Svenning JC, Thuiller W, Araujo MB, Guisan A, Zimmermann NE (2010) Biotic and abiotic variables show little redundancy in explaining tree species distributions. Ecography 33:1038–1048CrossRefGoogle Scholar
  42. 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
  43. Ministry for the Environment (2008) Climate change effects and impacts assessment: a guidance manual for local government in New Zealand, 2nd edn. Mullan B, Wratt D, Dean S, Hollis M, Allan S, Williams T, Kenny G (eds) Ministry for the Environment, WellingtonGoogle Scholar
  44. Moore P, Hawkins SJ, Thompson RC (2007) Role of biological habitat amelioration in altering the relative responses of congeneric species to climate change. Marine Ecol Prog Ser 334:11–19CrossRefGoogle Scholar
  45. Morin X, Lechowicz MJ (2008) Contemporary perspectives on the niche that can improve models of species range shifts under climate change. Biol Lett 4:573–576CrossRefPubMedGoogle Scholar
  46. Niedrist G, Bertoldi G, Della Chiesa S, Hell V, Tasser E, Tappeiner U (2011) Transplantation experiments in an inner-alpine dry valley to predict climate change effects on agriculturally used grassland ecosystem. In: Geophysical Research Abstracts, EGU General Assembly 2011, pp 10218–10218Google Scholar
  47. Norton LR, Firbank LG, Scott A, Watkinson AR (2005) Characterising spatial and temporal variation in the finite rate of population increase across the northern range boundary of the annual grass Vulpia fasciculata. Oecologia 144:407–415CrossRefPubMedGoogle Scholar
  48. Parmesan C (1996) Climate and species’ range. Nature 382:765–766CrossRefGoogle Scholar
  49. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefPubMedGoogle Scholar
  50. Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H, Huntley B, Kaila L, Kullberg J, Tammaru T, Tennent WJ, Thomas JA, Warren M (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583CrossRefGoogle Scholar
  51. Parmesan C, Gaines S, Gonzalez L, Kaufman DM, Kingsolver J, Townsend Peterson A, Sagarin R (2005) Empirical perspectives on species borders: from traditional biogeography to global change. Oikos 108:58–75CrossRefGoogle Scholar
  52. Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecol Biogeogr 12:361–371CrossRefGoogle Scholar
  53. Pearson RG, Dawson TP (2005) Long-distance plant dispersal and habitat fragmentation: identifying conservation targets for spatial landscape planning under climate change. Biol Conserv 123:389–401CrossRefGoogle Scholar
  54. Poloczanska ES, Hawkins SJ, Southward AJ, Burrows MT (2008) Modelling the response of populations of competing species to climate change. Ecology 89:3138–3149CrossRefGoogle Scholar
  55. Post E, Forchhammer MC (2008) Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos Transact R Soc B-Biol Sci 363:2369–2375Google Scholar
  56. Prince SD, Carter RN (1985) Topographical distribution of prickly lettuce (Lactuca serriola). III. Its performance in transplant sites beyond is distribution limit in Britain. J Ecol 73:49–64CrossRefGoogle Scholar
  57. R Development Core Team (2010) R: a language and environment for statistical computingGoogle Scholar
  58. Rutledge D (2003) Landscape indices as measures of the effects of fragmentation: can pattern reflect process?Google Scholar
  59. Schnitzler FR (2008) Hymenopteran parasitoid diversity and tri-trophic interactions: the effects of habitat fragmentation in Wellington. Victoria University of Wellington, New ZealandGoogle Scholar
  60. Schnitzler F-RR, Hartley S, Lester PJ (2011) Trophic-level responses differ at plant, plot, and fragment levels in urban native forest fragments: a hierarchical analysis. Ecol Entomol 36:241–250CrossRefGoogle Scholar
  61. Schweiger O, Settele J, Kudrna O, Klotz S, Kuhn I, Kühn I (2008) Climate change can cause spatial mismatch of trophically interacting species. Ecology 89:3472–3479CrossRefPubMedGoogle Scholar
  62. Silander JA, Klepeis DM (1999) The invasion ecology of Japanese barberry (Berberis thunbergii) in the New England landscape. Biol Invasions 1:189–201CrossRefGoogle Scholar
  63. Smith AC (1975) The genus Macropiper (Piperaceae). Bot J Linn Soc 71:1–38Google Scholar
  64. Spiller DM, Wise KAJ (1982) A catalogue (1860–1960) of New Zealand insects and their host plants. In: New Zealand Department of Scientific and Industrial Research, Wellington, NZGoogle Scholar
  65. Suttle KB, Thomsen MA, Power ME (2007) Species interactions reverse grassland responses to changing climate. Science 315:640–642CrossRefPubMedGoogle Scholar
  66. Svenning J-C, Skov F (2007) Could the tree diversity pattern in Europe be generated by postglacial dispersal limitation? Ecol Lett 10:453–460CrossRefPubMedGoogle Scholar
  67. The Native Plant Centre: New Zealand Native Plant Specialists (2007) The Native Plant Centre. 3rd December 2012. (
  68. Thomas CD (2010) Climate, climate change and range boundaries. Divers Distrib 16:488–495CrossRefGoogle Scholar
  69. Thomas CD, Lennon JJ (1999) Birds extend their ranges northwards. Nature 399:213CrossRefGoogle Scholar
  70. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363CrossRefPubMedGoogle Scholar
  71. Urban MC, Tewksbury JJ, Sheldon KS (2012) On a collision course: competition and dispersal differences create no-analogue communities and cause extinctions during climate change. In: Proceedings biological sciences/the Royal Society. Published online 4 January 2012Google Scholar
  72. van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578CrossRefGoogle Scholar
  73. van der Putten WH, Macel M, Visser ME (2010) Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos Trans R Soc B-Biol Sci 365:2025–2034CrossRefGoogle Scholar
  74. Wahl M, Link H, Alexandridis N, Thomason JC, Cifuentes M, Costello MJ, da Gama BAP, Hillock K, Hobday AJ, Kaufmann MJ, Keller S, Kraufvelin P, Kruger I, Lauterbach L, Antunes BL, Molis M, Nakaoka M, Nystrom J, bin Radzi Z, Stockhausen B, Thiel M, Vance T, Weseloh A, Whittle M, Wiesmann L, Wunderer L, Yamakita T, Lenz M (2011) Re-structuring of marine communities exposed to environmental change: a global study on the interactive effects of species and functional richness. PLoS ONE 6:e19514CrossRefPubMedGoogle Scholar
  75. Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB, Epstein HE, Jónsdóttir IS, Klein JA, Magnússon B, Molau U, Oberbauer SF, Rewa SP, Robinson CH, Shaver GR, Suding KN, Thompson CC, Tolvanen A, Totland Ø, Turner PL, Tweedie CE, Webber PJ, Wookey PA, Jonsdottir IS, Magnusson B, Totland O (2006) Plant community responses to experimental warming across the tundra biome. Proc Natl Acad Sci USA 103:1342–1346CrossRefPubMedGoogle Scholar
  76. Walther GR (2004) Plants in a warmer world. Perspect Plant Ecol Evol Syst 6:169–185CrossRefGoogle Scholar
  77. Willis SG, Hill JK, Thomas CD, Roy DB, Fox R, Blakeley DS, Huntley B (2009) Assisted colonization in a changing climate: a test-study using two UK butterflies. Conserv Lett 2:46–52CrossRefGoogle Scholar
  78. Wilmshurst JM, Anderson AJ, Higham TFG, Worthy TH (2008) Dating the late prehistoric dispersal of Polynesians to New Zealand using the commensal Pacific rat. PNAS 105:7676–7680CrossRefPubMedGoogle Scholar
  79. Winder M, Schindler DE (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106CrossRefGoogle Scholar
  80. Yang LH, Rudolf VHW (2010) Phenology, ontogeny and the effects of climate change on the timing of species interactions. Ecol Lett 13:1–10CrossRefPubMedGoogle Scholar
  81. Young A, Mitchell N (1994) Microclimate and vegetation edge effects in a fragmented podocarp-broadleaf forest in New Zealand. Biol Conserv 67:63–72CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Imperial College LondonAscotUK

Personalised recommendations