Oecologia

, Volume 157, Issue 3, pp 459–471

The invasive species Alliaria petiolata (garlic mustard) increases soil nutrient availability in northern hardwood-conifer forests

  • Vikki L. Rodgers
  • Benjamin E. Wolfe
  • Leland K. Werden
  • Adrien C. Finzi
Ecosystem Ecology - Original Paper

Abstract

The invasion of non-native plants can alter the diversity and activity of soil microorganisms and nutrient cycling within forests. We used field studies to analyze the impact of a successful invasive groundcover, Alliaria petiolata, on fungal diversity, soil nutrient availability, and pH in five northeastern US forests. We also used laboratory and greenhouse experiments to test three mechanisms by which A. petiolata may alter soil processes: (1) the release of volatile, cyanogenic glucosides from plant tissue; (2) the exudation of plant secondary compounds from roots; and (3) the decomposition of litter. Fungal community composition was significantly different between invaded and uninvaded soils at one site. Compared to uninvaded plots, plots invaded by A. petiolata were consistently and significantly higher in N, P, Ca and Mg availability, and soil pH. In the laboratory, the release of volatile compounds from the leaves of A. petiolata did not significantly alter soil N availability. Similarly, in the greenhouse, the colonization of native soils by A. petiolata roots did not alter soil nutrient cycling, implying that the exudation of secondary compounds has little effect on soil processes. In a leaf litter decomposition experiment, however, green rosette leaves of A. petiolata significantly increased the rate of decomposition of native tree species. The accelerated decomposition of leaf litter from native trees in the presence of A. petiolata rosette leaves shows that the death of these high-nutrient-content leaves stimulates decomposition to a greater extent than any negative effect that secondary compounds may have on the activity of the microbes decomposing the native litter. The results presented here, integrated with recent related studies, suggest that this invasive plant may change soil nutrient availability in such a way as to create a positive feedback between site occupancy and continued proliferation.

Keywords

Microbial diversity Nutrient cycling Biofumigation Root exudation Litter decomposition 

References

  1. Angeloni NL, Jankowski KJ, Tuchman NC, Kelly JJ (2006) Effects of an invasive cattail species (Typha × glauca) on sediment nitrogen and microbial community composition in a freshwater wetland. FEMS Microbiol Lett 263:86–92PubMedCrossRefGoogle Scholar
  2. Ashton IW, Hyatt LA, Howe KM, Gurevitch J, Lerdau MT (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous forest. Ecol Appl 15:1263–1272CrossRefGoogle Scholar
  3. Baruch Z, Goldstein G (1999) Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. Oecologia 121:183–192CrossRefGoogle Scholar
  4. Bialy Z, Oleszek W, Lewis J, Fenwick GR (1990) Allelopathic potential of glucosinolates (mustard oil glycosides) and their degradation products against wheat. Plant Soil 129:277–281Google Scholar
  5. Boon PI, Johnstone L (1997) Organic matter decay in coastal wetlands: an inhibitory role for essential oil from Melaleuca alternifolia leaves? Arch Hydrobiol 138:438–449Google Scholar
  6. Brown PD, Morra MJ (1997) Control of soil-borne plant pests using glucosinolates-containing plants. Adv Agron 61:167–231CrossRefGoogle Scholar
  7. Byers DL, Quinn JA (1998) Demographic variation in Alliaria petiolata (Brassicaceae) in four contrasting habitats. J Torrey Bot Soc 125:138–149CrossRefGoogle Scholar
  8. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290(5491):521–523PubMedCrossRefGoogle Scholar
  9. Cavers PB, Heagy MI, Kokron RF (1979) The biology of Canadian weeds. 35. Alliaria petiolata (M. Bieb.) Cavara and Grande. Can J Plant Sci 59:217–229CrossRefGoogle Scholar
  10. Chapin FSIII, Torn MS, Tateno M (1996) Principles of ecosystem sustainability. Am Nat 148:1016–1037CrossRefGoogle Scholar
  11. 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
  12. Cipollini D, Gruner B (2007) Cyanide in the chemical arsenal of garlic mustard, Alliaria petiolata. J Chem Ecol 33:85–94PubMedCrossRefGoogle Scholar
  13. D’Antonio C, Vitousek PM (1992) Biological invasions by exotic grasses, the grass fire cycle, and global change. Annu Rev Ecol Syst 23:63–87Google Scholar
  14. D’Antonio CM, Hughes FR, Mack M, Hitchcock D, Vitousek PM (1998) The response of native species to removal of invasive exotic grasses in a seasonally dry Hawaiian woodland. J Veg Sci 9:699–712CrossRefGoogle Scholar
  15. Degens BP, Harris JA (1997) Development of a physiological approach to measuring the catabolic diversity of soil microbial communities. Soil Biol Biochem 29:1309–1320CrossRefGoogle Scholar
  16. Duda JJ, Freeman DC, Emlen JM, Belnap J, Kitchen SG, Zak JC, Sobek E, Tracy M, Montane J (2003) Differences in native soil ecology associated with the invasion of the exotic annual chenopod, Halogenton glomeratus. Biol Fertil Soils 38:72–77CrossRefGoogle Scholar
  17. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523CrossRefGoogle Scholar
  18. Ehrenfeld JG, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300CrossRefGoogle Scholar
  19. Enloe SF, DiTomaso JM, Orloff SB, Drake DJ (2004) Soil water dynamics differ among rangeland plant communities dominated by yellow starthistle (Centaurea solstitialis), annual grasses, or perennial grasses. Weed Sci 52:929–935CrossRefGoogle Scholar
  20. Evans RD, Rimer R, Sperry L, Belnap J (2001) Exotic plant invasion alters nitrogen dynamics in an arid grassland. Ecol Appl 11:1301–1310CrossRefGoogle Scholar
  21. Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51PubMedCrossRefGoogle Scholar
  22. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118PubMedCrossRefGoogle Scholar
  23. Haribal M, Renwick JAA (1998) Isovitexin 6″-O-β-d-glucopyranoside: a feeding deterrent to Pieris napi oleracea from Alliaria petiolata. Phytochemistry 47:1237–1240CrossRefGoogle Scholar
  24. Haribal M, Yang Z, Attygalle AB, Renwick JAA, Meinwald J (2001) A cyanoallyl glucoside from Alliaria petiolata, as a feedling deterrent for larvae of Pieris napi oleracea. J Nat Prod 64:440–443PubMedCrossRefGoogle Scholar
  25. Hart SC, Binkley D (1984) Colorimetric interference and recovery of adsorbed ions from ion exchange resins. Commun Soil Sci Plant Anal 15:893–902CrossRefGoogle Scholar
  26. Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985CrossRefGoogle Scholar
  27. Hendershot WH, Lalande H, Duquette M (1993a) Soil reaction and exchangeable acidity. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis, New York, pp 141–145Google Scholar
  28. Hendershot WH, Lalande H, Duquette M (1993b) Ion exchange and exchangeable cations. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis, New York, pp 141–145Google Scholar
  29. Hofer S (2003) Determination of ammonia (salicylate) in 2 M KCl soil extracts by flow injection analysis. QuikChem method 12-107-06-2-A. Lachat Instruments, LovelandGoogle Scholar
  30. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:68–70CrossRefGoogle Scholar
  31. Knepel K (2003) Determination of nitrate in 2 M KCl soil extracts by flow injection analysis. QuikChem method 12-107-04-1-B. Lachat Instruments, LovelandGoogle Scholar
  32. Kourtev PS, Ehrenfeld JG, Huang W (1999) Differences in earthworm densities and nitrogen dynamics under exotic and native plant species. Biol Invas 1:237–245CrossRefGoogle Scholar
  33. Mack MC, D’Antonio CM (2003) The effects of exotic grasses on litter decomposition in a Hawaiian Woodland: the importance of indirect effects. Ecosystems 6:723–738CrossRefGoogle Scholar
  34. Mack MC, D’Antonio CM, Ley RE (2001) Alteration of ecosystem nitrogen dynamics by exotic plants: a case study of C4 grasses in Hawaii. Ecol Appl 11:1323–1335Google Scholar
  35. Mayton HS, Olivier C, Vaughn SF, Loria R (1996) Correlation of fungicidal activity of Brassica species with allyl isothiocyanate production in macerated leaf tissue. Phytopathology 86:267–271CrossRefGoogle Scholar
  36. McCarthy BC (1997) Response of a forest understory community to experimental removal of an invasive nonindigenous plant (Alliaria petiolata, Brassicaceae). In: Luken JO, Thieret JW (eds) Assessment and management of plant invasions. Springer, New York, pp 117–130Google Scholar
  37. Meekins JF, McCarthy BC (1999) Competitive ability of Alliaria petiolata (Garlic mustard, Brassicaceae), an invasive, nonindigenous forest herb. Int J Plant Sci 160:743–752CrossRefGoogle Scholar
  38. Meekins JF, McCarthy BC (2001) Effect of environmental variation on the invasive success of a nonindigenous forest herb. Ecol Appl 11:1336–1348CrossRefGoogle Scholar
  39. Mitchell RJ, Marrs RH, LeDuc MG, Auld MHD (1997) A study of succession on lowland heaths in Dorset, southern England: changes in vegetation and soil chemical properties. J Appl Ecol 34:1426–1444CrossRefGoogle Scholar
  40. Nagel JM, Griffin KL (2001) Construction cost and invasive potential: comparing Lythrum salicaria (Lythraceae) with co-occurring native species along pond banks. Am J Bot 88:2252–2258CrossRefGoogle Scholar
  41. Nahrstedt A (1985) Cyanogenesis and the role of cyanogenic compounds in insects. Plant Syst Evol 150:35–47CrossRefGoogle Scholar
  42. NCDC (2005) Climatological data annual summary New England 117. National Climate Data Center. http://www.ncdc.noaa.gov/
  43. Nuzzo VA (1993) Natural mortality of garlic mustard (Alliaria petiolata (Bieb) Cavara & Grande) rosettes. Nat Area J 13:132–133Google Scholar
  44. Nuzzo VA (1999) Invasion pattern of the herb garlic mustard (Alliaria petiolata) in high-quality forests. Biol Invas 1:169–179CrossRefGoogle Scholar
  45. Prati D, Bossdorf O (2004) Allelopathic inhibitition of germination by Alliaria petiolata (Brassicaceae). Am J Bot 91:285–288CrossRefGoogle Scholar
  46. Ralser M, Querfurth R, Warnatz HJ, Lehrach H, Yaspo M-L, Krobitsch S (2006) An efficient and economic enhancer mix for PCR. Biochem Biophys Res Commun 347:747–751PubMedCrossRefGoogle Scholar
  47. Rees GN, Baldwin DS, Watson GO, Perryman S, Nielson DL (2004) Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Antonie Van Leeuwenhoek 86:339–347PubMedCrossRefGoogle Scholar
  48. Schlesinger WH (1997) Biogeochemistry, an analysis of global change. Academic Press, New YorkGoogle Scholar
  49. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, New York, p 605Google Scholar
  50. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727–731CrossRefGoogle Scholar
  51. Stinson KA, Kaufman SK, Durbin L, Lowenstein F (2007) Impacts of garlic mustard invasion on a forest understory community. North East Nat 14:73–88CrossRefGoogle Scholar
  52. Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307CrossRefGoogle Scholar
  53. Tilman D, Knops J, Wedin D, Peter B, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302CrossRefGoogle Scholar
  54. Troelstra SR, Wagenaar R, Smant W, Peters BAM (2001) Interpretation of bioassays in the study of interactions between soil organisms and plants: involvement of nutrient factors. New Phytol 150:697–706CrossRefGoogle Scholar
  55. Vitousek PM, Walker LR, Whiteaker LD, Muellerdombois D, Matson PA (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804PubMedCrossRefGoogle Scholar
  56. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  57. Wilcove DS, Rothstein D, Bubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. BioScience 48(8):607–615CrossRefGoogle Scholar
  58. Wolfe BE, Rodgers VL, Stinson KA, Pringle A (2008) Ectomycorrhizal fungi communities are inhibited by the invasive plant Alliaria petiolata (garlic mustard). J Ecol 96:777–783CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Vikki L. Rodgers
    • 1
    • 2
  • Benjamin E. Wolfe
    • 3
  • Leland K. Werden
    • 1
  • Adrien C. Finzi
    • 1
  1. 1.Department of BiologyBoston UniversityBostonUSA
  2. 2.Math and Science DivisionBabson CollegeBabson ParkUSA
  3. 3.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA

Personalised recommendations