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.
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References
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 263:86–92
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 15:1263–1272
Baruch Z, Goldstein G (1999) Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. Oecologia 121:183–192
Bialy Z, Oleszek W, Lewis J, Fenwick GR (1990) Allelopathic potential of glucosinolates (mustard oil glycosides) and their degradation products against wheat. Plant Soil 129:277–281
Boon PI, Johnstone L (1997) Organic matter decay in coastal wetlands: an inhibitory role for essential oil from Melaleuca alternifolia leaves? Arch Hydrobiol 138:438–449
Brown PD, Morra MJ (1997) Control of soil-borne plant pests using glucosinolates-containing plants. Adv Agron 61:167–231
Byers DL, Quinn JA (1998) Demographic variation in Alliaria petiolata (Brassicaceae) in four contrasting habitats. J Torrey Bot Soc 125:138–149
Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290(5491):521–523
Cavers PB, Heagy MI, Kokron RF (1979) The biology of Canadian weeds. 35. Alliaria petiolata (M. Bieb.) Cavara and Grande. Can J Plant Sci 59:217–229
Chapin FSIII, Torn MS, Tateno M (1996) Principles of ecosystem sustainability. Am Nat 148:1016–1037
Cipollini D (2002) Variation in the expression of chemical defenses in Alliaria petiolata (Brassicaceae) in the field and common garden. Am J Bot 89:1422–1430
Cipollini D, Gruner B (2007) Cyanide in the chemical arsenal of garlic mustard, Alliaria petiolata. J Chem Ecol 33:85–94
D’Antonio C, Vitousek PM (1992) Biological invasions by exotic grasses, the grass fire cycle, and global change. Annu Rev Ecol Syst 23:63–87
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 9:699–712
Degens BP, Harris JA (1997) Development of a physiological approach to measuring the catabolic diversity of soil microbial communities. Soil Biol Biochem 29:1309–1320
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 38:72–77
Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523
Ehrenfeld JG, Kourtev P, Huang W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300
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 52:929–935
Evans RD, Rimer R, Sperry L, Belnap J (2001) Exotic plant invasion alters nitrogen dynamics in an arid grassland. Ecol Appl 11:1301–1310
Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Haribal M, Renwick JAA (1998) Isovitexin 6″-O-β-d-glucopyranoside: a feeding deterrent to Pieris napi oleracea from Alliaria petiolata. Phytochemistry 47:1237–1240
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 64:440–443
Hart SC, Binkley D (1984) Colorimetric interference and recovery of adsorbed ions from ion exchange resins. Commun Soil Sci Plant Anal 15:893–902
Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985
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 141–145
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 141–145
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, Loveland
Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:68–70
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, Loveland
Kourtev PS, Ehrenfeld JG, Huang W (1999) Differences in earthworm densities and nitrogen dynamics under exotic and native plant species. Biol Invas 1:237–245
Mack MC, D’Antonio CM (2003) The effects of exotic grasses on litter decomposition in a Hawaiian Woodland: the importance of indirect effects. Ecosystems 6:723–738
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 11:1323–1335
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 86:267–271
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 117–130
Meekins JF, McCarthy BC (1999) Competitive ability of Alliaria petiolata (Garlic mustard, Brassicaceae), an invasive, nonindigenous forest herb. Int J Plant Sci 160:743–752
Meekins JF, McCarthy BC (2001) Effect of environmental variation on the invasive success of a nonindigenous forest herb. Ecol Appl 11:1336–1348
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 34:1426–1444
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 88:2252–2258
Nahrstedt A (1985) Cyanogenesis and the role of cyanogenic compounds in insects. Plant Syst Evol 150:35–47
NCDC (2005) Climatological data annual summary New England 117. National Climate Data Center. http://www.ncdc.noaa.gov/
Nuzzo VA (1993) Natural mortality of garlic mustard (Alliaria petiolata (Bieb) Cavara & Grande) rosettes. Nat Area J 13:132–133
Nuzzo VA (1999) Invasion pattern of the herb garlic mustard (Alliaria petiolata) in high-quality forests. Biol Invas 1:169–179
Prati D, Bossdorf O (2004) Allelopathic inhibitition of germination by Alliaria petiolata (Brassicaceae). Am J Bot 91:285–288
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 347:747–751
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 86:339–347
Schlesinger WH (1997) Biogeochemistry, an analysis of global change. Academic Press, New York
Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, New York, p 605
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 4:727–731
Stinson KA, Kaufman SK, Durbin L, Lowenstein F (2007) Impacts of garlic mustard invasion on a forest understory community. North East Nat 14:73–88
Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307
Tilman D, Knops J, Wedin D, Peter B, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302
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 150:697–706
Vitousek PM, Walker LR, Whiteaker LD, Muellerdombois D, Matson PA (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804
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 315–322
Wilcove DS, Rothstein D, Bubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. BioScience 48(8):607–615
Wolfe BE, Rodgers VL, Stinson KA, Pringle A (2008) Ectomycorrhizal fungi communities are inhibited by the invasive plant Alliaria petiolata (garlic mustard). J Ecol 96:777–783
Acknowledgements
We would like to thank Eddie Brzostek, Anne Gallet Budynek, Jenny Talbot, Meredith Zaccherio, Bridgid Curry, Shaheen Kanchwala, Sharon Hyzy, and Colin Averill for laboratory and field assistance. In addition we thank the Great Mountain Forest Corporation, the Childs family, the Bridgeport Hydraulic Company and the Norfolk Land Trust for the use of their land. Jody Bronson, Russell Russ and Frank Christinat also provided valuable support. Finally we would like to thank Anne Gallet Budynek, Eddie Brzostek, Colin Orians and Pamela Templer for their helpful comments on earlier drafts of this manuscript. This research was supported by a grant from the USDA. Additional support for this research was provided to V. L. R. by an NSF Doctoral Dissertation Improvement Grant and also by the Sigma Xi program Grants in Aid of Research. The experiments conducted here comply with the current laws of the United States.
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Communicated by Hormoz BassiriRad.
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Rodgers, V.L., Wolfe, B.E., Werden, L.K. et al. The invasive species Alliaria petiolata (garlic mustard) increases soil nutrient availability in northern hardwood-conifer forests. Oecologia 157, 459–471 (2008). https://doi.org/10.1007/s00442-008-1089-8
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DOI: https://doi.org/10.1007/s00442-008-1089-8