Oecologia

, Volume 148, Issue 3, pp 384–395 | Cite as

Geographic patterns of herbivory and resource allocation to defense, growth, and reproduction in an invasive biennial, Alliaria petiolata

  • Kristin C. Lewis
  • F.A. Bazzaz
  • Qing Liao
  • Colin M. Orians
Ecophysiology

Abstract

We investigated geographic patterns of herbivory and resource allocation to defense, growth, and reproduction in an invasive biennial, Alliaria petiolata, to test the hypothesis that escape from herbivory in invasive species permits enhanced growth and lower production of defensive chemicals. We quantified herbivore damage, concentrations of sinigrin, and growth and reproduction inside and outside herbivore exclusion treatments, in field populations in the native and invasive ranges. As predicted, unmanipulated plants in the native range (Hungary, Europe) experienced greater herbivore damage than plants in the introduced range (Massachusetts and Connecticut, USA), providing evidence for enemy release, particularly in the first year of growth. Nevertheless, European populations had consistently larger individuals than US populations (rosettes were, for example, eightfold larger) and also had greater reproductive output, but US plants produced larger seeds at a given plant height. Moreover, flowering plants showed significant differences in concentrations of sinigrin in the invasive versus native range, although the direction of the difference was variable, suggesting the influence of environmental effects. Overall, we observed less herbivory, but not increased growth or decreased defense in the invasive range. Geographical differences in performance and leaf chemistry appear to be due to variation in the environment, which could have masked evolved differences in allocation.

Keywords

Alliaria petiolata EICA Herbivory Invasive species Sinigrin 

Notes

Acknowledgements

This work was funded by a NSF Graduate Student Fellowship and an EPA STAR Fellowship to KCL, as well as a Harvard OEB Student Dissertation Grant and the Massachusetts Natural Heritage and Endangered Species Program. Peter Ashton, Missy Holbrook, Brooke Parry-Hecht, Naomi Pierce, Bernhard Schmid, Amity Wilczek and Kelly Wolfe-Bellin and four anonymous reviewers provided helpful comments on previous versions of this manuscript. We thank the Duna-Ipoly and Bükk National Park directorates, Trustees of Reservations, and National Audubon, and Harvard Forest for use of research sites. Francie Chew provided assistance with the HPLC-MS column and chemical extraction protocol. We thank Sylvan Kaufman, János Nagy, András Schmotzer, Kristina Stinson, Rich Stomberg, and Zoltán Tuba for assistance with the field studies. Aaron Ellison provided feedback on statistical analyses, but any errors are the authors’ own. Special thanks to our research assistants: Dan Flynn, Daria Hinz, Julia Mansfield, and Luke McKneally. Samples were transported under USDA Permit # 37–83868.

References

  1. Anderson R, Dhillion S, Kelley T (1996) Aspects of the ecology of an invasive plant, garlic mustard (Alliaria petiolata), in central Illinois. Restor Ecol 4:181–191CrossRefGoogle Scholar
  2. Bardon R, Countryman D, Hall R (1995) A reassessment of using light-sensitive diazo paper for measuring integrated light in the field. Ecology 76:1013–1016CrossRefGoogle Scholar
  3. Bazzaz F, Chiariello N, Coley P, Pitelka L (1987) Allocating resources to reproduction and defense. BioScience 37:58–67CrossRefGoogle Scholar
  4. Bernays EA, Oppenheim S, Chapman RF, Kwon H, Gould F (2000) Taste sensitivity of insect herbivores to deterrents is greater in specialists than in generalists: a behavioral test of the hypothesis with two closely related caterpillars. J Chem Ecol 26:547–563CrossRefGoogle Scholar
  5. Blossey B, Nuzzo V, Hinz HL, Gerber E (2001) Developing biological control of Alliaria petiolata (M. Bieb.) Cavara and Grande (garlic mustard). Nat Areas J 21:3570367Google Scholar
  6. Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889CrossRefGoogle Scholar
  7. Booth E, Walker K, Griffiths D (1990) Effect of harvest date and pod position on glucosinolates in oilseed rape (Brassica napus). J Sci Food Agric 53:43–61CrossRefGoogle Scholar
  8. Bossdorf O, Prati D, Auge H, Schmid B (2004) Reduced competitive ability in an invasive plant. Ecol Lett 7:346–353CrossRefGoogle Scholar
  9. Byers D, Quinn J (1998) Demographic variation in Alliaria petiolata (Brassicaceae) in four contrasting habitats. J Torrey Bot Soc 125:138–149CrossRefGoogle Scholar
  10. Carson W, Root R (1999) Top-down effects of insect herbivores during early succession: influence on biomass and plant dominance. Oecologia 121:260–272CrossRefGoogle Scholar
  11. Cavers P, Heagy M, Kokron R (1979) The biology of Canadian weeds. 35. Alliaria petiolata (M. Bieb.) Cavara and Grande. Can J Plant Sci 59:217–229CrossRefGoogle Scholar
  12. Cipollini D (2002) Variation in the expression of chemical defenses in Alliaria petiolata (Brassicaceae) in the field and common garden. Am J Bot 89:1422–1430CrossRefGoogle Scholar
  13. Ciska E, Martyniak-Przybyszewska B, Kozlowska H (2000) Content of glucosinolates in cruciferous vegetables grown at the same site for two years under different climatic conditions. J Agric Food Chem 48:2862–2867CrossRefPubMedGoogle Scholar
  14. Clossais-Besnard N, Larher F (1991) Physiological role of glucosinolates in Brassica napus. Concentration and distribution pattern of glucosinolates among plant organs during a complete life cycle. J Sci Food Agric 56:25–38CrossRefGoogle Scholar
  15. Crawley M (1987) What makes a community invasible? In: Gray A, Crawley M, Edwards P (eds) Colonization, succession, and stability. Blackwell,, Oxford, pp 429–453Google Scholar
  16. Cruden R, McClain A, Shrivastava G (1996) Pollination biology and breeding system of Alliaria petiolata (Brassicaceae). Bull Torrey Bot Club 123:273–280CrossRefGoogle Scholar
  17. Daehler C (1998) The taxonomic distribution of invasive angiosperm plants: ecological insights and comparison to agricultural weeds. Biol Conserv 84:167–180CrossRefGoogle Scholar
  18. Daehler C, Strong D (1997) Reduced herbivore resistance in introduced smooth cordgrass (Spartina alterniflora) after a century of herbivore-free growth. Oecologia 110:99–108CrossRefGoogle Scholar
  19. Daxenbichler M, Spencer G, Carlson D, Rose G, Brinker A, Powell R (1991) Glucosinolate composition of seeds from 297 species of wild plants. Phytochemistry 30:2623–2638CrossRefGoogle Scholar
  20. Elton C (2000) The ecology of invasions by animals and plants, 2nd edn. University of Chicago Press, ChicagoGoogle Scholar
  21. Feeny P, Rosenberry L (1982) Seasonal variation in the glucosinolate content of North American Brassica nigra and Dentaria species. Biochem Syst Ecol 10:23–32CrossRefGoogle Scholar
  22. Friend D (1961) A simple method of measuring integrated light values in the field. Ecology 42:577–580CrossRefGoogle Scholar
  23. Hacia H, Vitale CS, Arkin MA, McKittrick DA (1991) Climates of the World. In: National oceanic and atmospheric administration, Asheville, North Carolina, pp 40Google Scholar
  24. Herms D, Mattson W (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  25. Huang X, Renwick J (1994) Relative activities of glucosinolates as oviposition stimulants for Pieris rapae and P. napi oleracea. J Chem Ecol 20:1025–1037CrossRefGoogle Scholar
  26. Hunter M, Schultz J (1995) Fertilization mitigates chemical induction and herbivore responses within damaged oak trees. Ecology 76:1226–1232CrossRefGoogle Scholar
  27. Jalas J, Suominen J (eds) (1994) Atlas Florae Europaeae: distribution of vascular plants in Europe. Committee for Mapping the Flora of Europe, HelsinkiGoogle Scholar
  28. Louda S, Collinge S (1992) Plant resistance to insect herbivores: a field test of the environmental stress hypothesis. Ecology 73:153–169CrossRefGoogle Scholar
  29. Louda S, Mole S (1991) Glucosinolates: chemistry and ecology. In: Rosenthal G, Berenbaum M (eds) Herbivores: their interactions with secondary plant metabolites, vol 1: The Chemical Participants, 2nd edn. Academic, San Diego, pp 123–164Google Scholar
  30. Maron JL, Vilá M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280CrossRefGoogle Scholar
  31. McGlynn T (1999) The worldwide transfer of ants: geographical distribution and ecological invasions. J Biogeogr 26:535–548CrossRefGoogle Scholar
  32. Meekins J, McCarthy B (1999) Competitive ability of Alliaria petiolata (garlic mustard, Brassicaceae), an invasive, nonindigenous forest herb. Int J Plant Sci 160:743–752CrossRefGoogle Scholar
  33. Mitchell C, Power A (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627PubMedCrossRefGoogle Scholar
  34. Nichols-Orians C, Schultz J (1990) Interactions among leaf toughness, chemistry, and harvesting by attine ants. Ecol Entomol 15:311–320CrossRefGoogle Scholar
  35. Nuzzo V (1993) Distribution and spread of the invasive biennial Alliaria petiolata (garlic mustard) in North America. In: McKnight B (ed) Biological pollution: the control and impact of invasive exotic species. Indiana Academy of Science, Indianapolis, pp 137–145Google Scholar
  36. Pivnick K, Lamb R, Reed D (1992) Response of flea beetles, Phyllotreta spp., to mustard oils and nitriles in field trapping experiments. J Chem Ecol 18:863–873CrossRefGoogle Scholar
  37. Rejmánek M (2000) Invasive plants: approaches and predictions. Aust Ecol 25:497–506CrossRefGoogle Scholar
  38. Renwick JAA, Zhang W, Haribal M, Attygalle AB, Lopez KD (2001) Dual chemical barriers protect a plant against different larval stages of an insect. J Chem Ecol 27:1575–1583CrossRefPubMedGoogle Scholar
  39. Siemann E, Rogers W (2001) Genetic differences in growth of an invasive tree species. Ecol Lett 4:514–518CrossRefGoogle Scholar
  40. Soerensen H (1990) Glucosinolates- structure, properties, function. In: Shahidi F (ed) Canola and rapeseed. van Nostrand Reinhold, New York, pp 149–172Google Scholar
  41. Szentesi Á (1990) Controversial components of plant apparency in Alliaria petiolata Cavara & Grande (Cruciferae). In: Szentesi Á, Jermy T (eds) Insects-plants ‘89, vol 39. Akadémiai Kiadó, Budapest, pp 237–244Google Scholar
  42. Thébaud C, Simberloff D (2001) Are plants really larger in their introduced ranges? Am Nat 157:231–236CrossRefPubMedGoogle Scholar
  43. Torchin M, Lafferty K, Dobson A, McKenzie V, Kurls A (2003) Introduced species and their missing parasites. Nature 421:628–630PubMedCrossRefGoogle Scholar
  44. Traw MB, Dawson TE (2002) Reduced performance of two specialist herbivores (Lepidoptera: Pieridae, Coleoptera: Chrysomelidae) on new leaves of damaged black mustard plants. Environ Entomol 31:714–722CrossRefGoogle Scholar
  45. Troyer J, Stephenson K, Fahey J (2001) Analysis of glucosinolates from broccoli and other cruciferous vegetables by hydrophilic interaction liquid chromatography. J Chromatogr A 919:299–304CrossRefPubMedGoogle Scholar
  46. USDA, NRCS (2002) The PLANTS Database, Version 3.5. In, vol. 2003. National Plant Data Center, Baton Rouge, LA 70874–4490 USAGoogle Scholar
  47. van Kleunen M, Schmid B (2003) No evidence for an evolutionary increased competitive ability in an invasive plant. Ecology 84:2816–2823CrossRefGoogle Scholar
  48. Vaughn S, Berhow M (1999) Allelochemicals isolated from tissues of the invasive weed garlic mustard (Alliaria petiolata). J Chem Ecol 25:2495–2504CrossRefGoogle Scholar
  49. Weatherbee P, Somers P, Simmons T (1998) A guide to invasive plants in Massachusetts. In. Massachusetts Biodiversity Initiative, Massachusetts Division of Fisheries and Wildlife, BostonGoogle Scholar
  50. Williamson M, Fitter A (1996) The characters of successful invaders. Biol Conserv 78:163–170CrossRefGoogle Scholar
  51. Willis A, Thomas M, Lawton J (1999) Is the increased vigour of invasive weeds explained by a trade-off between growth and herbivore resistance? Oecologia 120:632–640CrossRefGoogle Scholar
  52. Willis AJ, Memmott J, Forrester RI (2000) Is there evidence for the post-invasion evolution of increased size among invasive plant species? Ecol Lett 3:275–283CrossRefGoogle Scholar
  53. Wolfe L (2002) Why alien invaders succeed: support for the escape-from-enemy hypothesis. Am Nat 160:705–711CrossRefPubMedGoogle Scholar
  54. Zangerl A, Bazzaz F (1992) Theory and pattern in plant defense allocation. In: Fritz R, Simms E (eds) Plant resistance to herbivores and pathogens: ecology, evolution and genetics. Chicago University Press, Chicago, pp 363–391Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Kristin C. Lewis
    • 1
    • 4
  • F.A. Bazzaz
    • 1
  • Qing Liao
    • 2
  • Colin M. Orians
    • 3
  1. 1.Department of Organismic and Evolutionary BiologyBiological LaboratoriesCambridgeUSA
  2. 2.Harvard Mass Spectrometry Facility, Chemistry and Chemical BiologyHarvard UniversityCambridgeUSA
  3. 3.Department of BiologyTufts UniversityMedfordUSA
  4. 4.Rowland Institute at HarvardCambridgeUSA

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