Abstract
Background and aims
Invasive plants have been associated with alterations to soil properties, functions, and organisms, with the potential to impact ecosystem processes. An observational study was conducted to determine how the invasive plant Frangula alnus affects soil microbial communities and biogeochemical processes in Wisconsin forests.
Methods
Paired invaded/non-invaded sites (n = 10), including high (n = 5) and low (n = 5) density invasions, were sampled in spring, summer, and fall. Soil was analyzed for extractable and total nitrogen (N), N mineralization rate, total carbon, microbial biomass carbon and N, and microbial community structure using terminal restriction fragment length polymorphisms.
Results
Linear regression analysis with robust variance estimation revealed higher N mineralization rates in invaded sites than non-invaded sites in summer, and in high density invaded sites than non-invaded sites overall (p < 0.05). There was not a corresponding increase in extractable N. No differences between invaded and non-invaded sites were observed for other variables.
Conclusions
Nitrogen-rich F. alnus leaf litter (3.2 % of dry mass) may contribute to elevated N mineralization at these sites, though pre-existing conditions may be responsible. Results suggest that F. alnus alters N cycling but has little impact on soil carbon pools and microbial communities.
Similar content being viewed by others
References
Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai’i. Oecologia 14:612–619
APHA-AWWA-WEF (1998) Standard methods for the examination of water and wastewater, 20th edn. Am Public Health Assoc, New York
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
Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8:217–230
Blair BC, Stowasser A (2009) Impact of Lonicera maackii on decomposition rates of native leaf litter in a southwestern Ohio woodland. Ohio J Sci 109:43–47
Boerner REJ (1984) Foliar nutrient dynamics and nutrient-use efficiency of four deciduous tree species in relation to site fertility. J Appl Ecol 21:1029–1040
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 6:837–842
Burke IC, Bontti EE, Barrett JE, Lowe PN, Lauenroth WK, Riggle R (2013) Impact of labile and recalcitrant carbon treatments on available nitrogen and plant communities in a semiarid ecosystem. Ecol Appl 23:537–545
Catling PM, Porebski ZS (1994) The history of invasion and current status of glossy buckthorn, Rhamnus frangula, in southern Ontario. Can Field Nat 108:305–310
Corbin JD, D’Antonio CM (2004) Effects of exotic species on soil nitrogen cycling: implications for restoration. Weed Technol 18:1464–1467
Czarapata EJ (2005) Invasive plants of the upper Midwest: an illustrated guide to their identification and control. The Univ of Wis Press, Madison
Day PR (1965) Particle fractionation and particle size analysis. In: Black CA (ed) Methods of soil analysis, part I: physical and mineralogical properties, including statistics of measurement and sampling. Am Soc of Agron, Madison, pp. 545–567
Drenovsky RE, Batten KM (2007) Invasion by Aegilops triuncialis (barb goatgrass) slows carbon and nutrient cycling in a serpentine grassland. Biol Invasions 9:107–116
Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523
Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80
Ehrenfeld JG, Kourtev PS, Huang W (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300
Elgersma KJ, Ehrenfeld JG, Yu S, Vor T (2011) Legacy effects overwhelm the short-term effects of exotic plant invasion and restoration on soil microbial community structure, enzyme activities, and nitrogen cycling. Oecologia 167:733–745
Escudero A, del Arco JM, Sanz IC, Ayala J (1992) Effects of leaf longevity and retranslocation efficiency on the retention time of nutrients in the leaf biomass of different woody species. Oecologia 90:80–87
Fagan ME, Peart DR (2004) Impact of the invasive shrub glossy buckthorn (Rhamnus frangula L.) on juvenile recruitment by canopy trees. For Ecol Manag 194:95–107
Follstad Shah JJ, Harner MJ, Tibbets TM (2010) Elaeagnus angustifolia elevates soil inorganic nitrogen pools in riparian ecosystems. Ecosystems 13:46–61
Frappier B, Eckert RT, Lee TD (2003) Potential impacts of the invasive exotic shrub Rhamnus frangula L. (glossy buckthorn) on forests of southern New Hampshire. Northeast Nat 10:277–296
Frappier B, Eckert RT, Lee TD (2004) Experimental removal of the non-indigenous shrub Rhamnus frangula (glossy buckthorn): effects on native herbs and woody seedlings. Northeast Nat 11:333–342
Fridley JD (2012) Extended leaf phenology and the autumn niche in deciduous forest invasions. Nature 485:359–364
Gleason HA, Cronquist A (1991) Manual of vascular plants of northeastern United States and adjacent Canada. New York Bot Gard, New York
Godwin H (1943) Frangula alnus Miller. J Ecol 31:77–92
Godwin H, Clowes DR, Huntley B (1974) Studies in the ecology of Wicken Fen V. Development of fen carr. J Ecol 62:197–214
Heneghan L, Clay C, Brundage C (2002) Rapid decomposition of buckthorn litter may change soil nutrient levels. Ecol Restor 20:108–111
Heneghan L, Fatemi F, Umek L, Grady K, Fagen K, Workman M (2006) The invasive shrub European buckthorn (Rhamnus cathartica, L.) alters soil properties in Midwestern U. S. Woodlands. Appl Soil Ecol 32:142–148
Kang H, Xin Z, Berg B, Burgess PJ, Liu Q, Liu Z, Li Z, Liu C (2010) Global pattern of leaf litter nitrogen and phosphorus in woody plants. Ann For Sci 67:811
Keeney DR, Nelson DW (1982) Nitrogen—inorganic forms. In: Page AL (ed) Methods of soil analysis. Part 2. Chemical and microbiological properties. Am Soc of Agron, Soil Sci Soc of Am, Madison, pp. 643–698
Kettenring MK, Adams CR (2011) Lessons learned from invasive plant control experiments: a systematic review and meta-analysis. J Appl Ecol 48:970–979
Klionsky SM, Amatangelo KL, Waller DM (2010) Above- and belowground impacts of European buckthorn (Rhamnus cathartica) on four native forbs. Restor Ecol 19:1–10
Kourtev PS, Ehrenfeld JG, Haggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166
Lee DW, Keefe JO, Holbrook NM, Field TS (2003) Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA. Ecol Res 18:677–694
Leishman MR, Haslehurst T, Ares A, Baruch Z (2007) Leaf trait relationships of native and invasive plants: community-and global-scale comparisons. New Phytol 176:635–643
Liao C, Peng R, Luo Y, Zhou X, Wu X, Fang C, Chen J, Li B (2008) Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytol 177:706–714
Liu WT, Marsh TL, Cheng H, Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63:4516–4522
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
Malicky H, Sobhian R, Zwolfer H (1970) Investigations on the possibilities of a biological control of Rhamnus cathartica L. in Canada: Host ranges, feeding sites, and phenology of insects associated with European Rhamnaceae. Z Angew Entomol 65:77–97
McEwan RW, Arthur MA, Alverson SE (2014) Throughfall chemistry and soil nutrient effects of the invasive shrub Lonicera maackii in deciduous forests. Am Midl Nat 168:43–55
Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626
Morel JG, Bokossa MC, Neerchal NK (2003) Small sample correction for the variance of GEE estimators. Biom J 4:395–409
Perry LG, Blumenthal DM, Monaco TA, Paschke MW, Redente EF (2010) Immobilizing nitrogen to control plant invasions. Oecologia 163:13–24
Pyšek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Ecological studies, vol 193. Springer, Berlin, pp. 97–125
Saggar S, McIntosh PD, Hedley CB, Knicker H (1999) Changes in soil microbial biomass, metabolic quotient, and organic matter turnover under Hieracium (H. pilosella, L.). Biol Fertil Soils 30:232–238
Scott NA, Binkley D (1997) Foliage litter quality and annual net nitrogen mineralization: comparison across north American forest sites. Oecologia 111:151–159
Stokdyk JP, Herrman KS (2014) Short-term impacts of Frangula alnus litter on forest soil properties. Water Air Soil Pollut 225:2000
Tappeiner JC, Alm AA (1975) Undergrowth vegetation effects on the nutrient content of litterfall and soils in red pine and birch stands in northern Minnesota. Ecology 56:1193–1200
Valery L, Bouchard V, Lefeuvre JC (2004) Impact of the invasive native species Elymus athericus on carbon pools in a salt marsh. Wetlands 24:268–276
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass carbon. Soil Biol Biochem 19:703–707
Vinton MA, Burke IC (1995) Interactions between individual plant species and soil nutrient status in shortgrass steppe. Ecology 76:1116–1133
Vinton MA, Goergen EM (2006) Plant–soil feedbacks contribute to the persistence of Bromus inermis in tallgrass prairie. Ecosystems 9:967–976
Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487
Acknowledgments
We thank the private landowners, Midstate Technical College, the cities of Stevens Point and Wausau, and Portage, Marathon, and Wood counties for granting access to study sites. We also thank Hunter Gosda and Alyssa Gunderson for their help in the field and lab, Keith Turnquist for assistance with TRFLP analysis, and Burney Kieke for assistance with modeling.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This study was funded by a McIntire-Stennis Cooperative Forestry Research Program grant (WIS01687) and the Gutgsell Family Foundation.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Klaus Butterbach-Bahl.
Electronic supplementary material
ESM 1
(PDF 85 kb)
Rights and permissions
About this article
Cite this article
Stokdyk, J.P., Herrman, K.S. Effects of Frangula alnus on soil microbial communities and biogeochemical processes in Wisconsin forests. Plant Soil 409, 65–75 (2016). https://doi.org/10.1007/s11104-016-2916-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-016-2916-z