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Non-native liana, Euonymus fortunei, associated with increased soil nutrients, unique bacterial communities, and faster decomposition rate

Abstract

Invasive plants have wide-ranging impacts on native systems including reducing native plant richness and altering soil chemistry, microbes, and nutrient cycling. Increasingly, these effects are found to linger long after removal of the invader. We examined how soil chemistry, bacterial communities, and litter decomposition varied with cover of Euonymus fortunei, an invasive evergreen liana, in two central Kentucky deciduous forests. In one forest, E. fortunei invaded in the late 1990s but invasion remained patchy and we paired invaded and uninvaded plots to examine the associations between E. fortunei cover and our response variables. In the second forest, E. fortunei had completely invaded the forest by 2005; areas where it had been selectively removed by 2010 were paired with an adjacent invaded plot. Where E. fortunei had patchily invaded, E. fortunei patches had up to 3.5× nitrogen, 2.7× carbon, and 1.9× more labile glomalin in soils than uninvaded plots, whereas there were no differences in soil characteristics between invaded and removal plots. In the patchily invaded forest, bacterial community composition varied among invaded and non-invaded plots, whereas bacterial communities did not vary among invaded and removal plots. Finally, E. fortunei leaf litter decomposed faster (k = 4.91 year−1) than the native liana (k = 3.77 year−1), Vitis vulpina; decomposition of both E. fortunei and V. vulpina was faster in invaded (k = 7.10 year−1) than removal plots (k = 4.77 year−1). Our findings suggest that E. fortunei invasion increases the rate of leaf litter decomposition via high-quality litter, alters the decomposition environment, and shifts in the soil biotic communities associated with a dense mat of wintercreeper. Land managers with limited resources should target the densest mats for the greatest restoration potential and remove wintercreeper patches before they establish dense mats.

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References

  • Arthur M, Bray S, Kuchle C, McEwan R (2012) The influence of the invasive shrub, Lonicera maackii, on leaf decomposition and microbial community dynamics. Plant Ecol 213:1571–1582

    Article  Google Scholar 

  • Ashton IW, Hyatt LA, Howe KM, Gurevitch J, Lerdau MT (2005) Invasive species accelerate decomposition and litter nitrogen loss in a mixed deciduous. Ecol Appl 15:1263–1272. doi:10.1890/04-0741

    Article  Google Scholar 

  • Asner GP, Martin RE (2012) Contrasting leaf chemical traits in tropical lianas and trees: implications for future forest composition. Ecol Lett 15:1001–1007. doi:10.1111/j.1461-0248.2012.01821.x

    Article  PubMed  Google Scholar 

  • Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WA, Knight R, Fierer N (2011) The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43:1450–1455. doi:10.1016/j.soilbio.2011.03.012

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc B Biol Sci 269:2595–2601. doi:10.1098/rspb.2002.2162

    Article  Google Scholar 

  • Bloom TC, Baskin JM, Baskin CC (2002) Ecological life history of the facultative woodland biennial Arabis laevigata variety laevigata (Brassicaceae): seed dispersal. J Torrey Bot Soc 129:21–28. doi:10.2307/3088679

    Article  Google Scholar 

  • Bray SR, Kitajima K, Sylvia DM (2003) Mycorrhizae differentially alter growth, physiology, and competitive ability of an invasive shrub. Ecol Appl 13:565–574. doi:10.1890/1051-0761(2003)013[0565:MDAGPA]2.0.CO;2

    Article  Google Scholar 

  • Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. doi:10.1038/ismej.2012.8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Carey CJ, Beman JM, Eviner VT, Malmstrom CM, Hart SC (2015) Soil microbial community structure is unaltered by plant invasion, vegetation clipping, and nitrogen fertilization in experimental semi-arid grasslands. Front Microbiol. doi:10.3389/fmicb.2015.00466

    Google Scholar 

  • Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:141–145. doi:10.1093/nar/gkn879

    Article  Google Scholar 

  • Cornelissen JHC, Thompson K (1997) Functional leaf attributes predict litter decomposition rate in herbaceous plants. New Phytol 135:109–114

    Article  Google Scholar 

  • Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, Van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Díaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071. doi:10.1111/j.1461-0248.2008.01219.x

    Article  PubMed  Google Scholar 

  • Couteaux M-M, Bottner P, Berg B (1995) Litter decomposition, climate and liter quality. Trends Ecol Evol 10:63–66. doi:10.1016/S0169-5347(00)88978-8

    CAS  Article  PubMed  Google Scholar 

  • D’Angelo E, Crutchfield J, Vandiviere M (2001) Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Qual 30:2206–2209

    Article  PubMed  Google Scholar 

  • Ehrenfeld JG, Kourtev P, Huang WZ (2001) Changes in soil functions following invasions of exotic understory plants in deciduous forests. Ecol Appl 11:1287–1300

    Article  Google Scholar 

  • Elgersma KJ, Ehrenfeld JG, Yu S, Vor T (2011) Legacy effects overwhelm the short-term effect of exotic platn invasion and restoration on soil microbial community structure, enzyme activities, and nitrogen cycling. Oecologia 167:733–745

    Article  PubMed  Google Scholar 

  • Feng YL, Fu GL, Zheng YL (2008) Specific leaf area relates to the differences in leaf construction cost, photosynthesis, nitrogen allocation, and use efficiencies between invasive and noninvasive alien congeners. Planta 228:383–390. doi:10.1007/s00425-008-0732-2

    CAS  Article  PubMed  Google Scholar 

  • Fierer N, Bradford M, Jackson R (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364

    Article  PubMed  Google Scholar 

  • Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017. doi:10.1038/ismej.2011.159

    CAS  Article  PubMed  Google Scholar 

  • Ghani A, Dexter M, Perrott KW (2003) Hot-water extractable carbon in soils: a sensitive measurement for determining impacts of fertilisation, grazing and cultivation. Soil Biol Biochem 35:1231–1243. doi:10.1016/S0038-0717(03)00186-X

    CAS  Article  Google Scholar 

  • Hartman KM, McCarthy BC (2004) Restoration of a forest understory after the removal of an invasive shrub, Amur Honeysuckle (Lonicera maackii). Restor Ecol 12:154–165. doi:10.1111/j.1061-2971.2004.00368.x

    Article  Google Scholar 

  • Heberling JM, Fridley JD (2013) Functional traits and resource-use strategies of native and invasive plants in Eastern North American forests. New Phytol 200:523–533

    CAS  Article  PubMed  Google Scholar 

  • 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. doi:10.1016/j.apsoil.2005.03.009

    Article  Google Scholar 

  • Holub SM, Lajtha K, Spears JDH, Tóth JA, Crow SE, Caldwell BA, Papp M, Nagy PT (2005) Organic matter manipulations have little effect on gross and net nitrogen transformations in two temperate forest mineral soils in the USA and central Europe. For Ecol Manag 214:320–330. doi:10.1016/j.foreco.2005.04.016

    Article  Google Scholar 

  • Hutchison M (1992) Vegetation management guideline—Wintercreeper or climbing Euonymus (Euonymus-fortunei). Nat Areas J 12:220–221

    Google Scholar 

  • Iannone BV, Heneghan L, Rijal D, Wise DH (2015) Below-ground causes and consequences of woodland shrub invasions: a novel paired-point framework reveals new insights. J Appl Ecol 52:78–88. doi:10.1111/1365-2664.12354

    CAS  Article  Google Scholar 

  • Jo I, Fridley JD, Frank DA (2015) Linking above- and belowground resource use strategies for native and invasive species of temperate deciduous forests. Biol Invasions 17:1545–1554. doi:10.1007/s10530-014-0814-y

    Article  Google Scholar 

  • Jo I, Fridley JD, Frank DA (2016) More of the same? In situ leaf and root decomposition rates do not vary between 80 native and nonnative deciduous forest species. New Phytol 209:115–122. doi:10.1111/nph.13619

    CAS  Article  PubMed  Google Scholar 

  • Keith AM, Brooker RW, Osler GHR, Chapman SJ, Burslem DFRP, van der Wal R (2009) Strong impacts of belowground tree inputs on soil nematode trophic composition. Soil Biol Biochem 41:1060–1065. doi:10.1016/j.soilbio.2009.02.009

    CAS  Article  Google Scholar 

  • Kulmatiski A, Beard KH (2011) Long-term plant growth legacies overwhelm short-term plant growth effects on soil microbial community structure. Soil Biol Biochem 43:823–830. doi:10.1016/j.soilbio.2010.12.018

    CAS  Article  Google Scholar 

  • Lankau RA, Bauer JT, Anderson MR, Anderson RC (2014) Long-term legacies and partial recovery of mycorrhizal communities after invasive plant removal. Biol Invasions 16:1979–1990. doi:10.1007/s10530-014-0642-0

    Article  Google Scholar 

  • Leicht-Young SA, Pavlovic NB (2014) Lianas as invasive species in North America. In: Ecology of Lianas. pp 429–442

  • Leicht-Young SA, O’Donnell H, Latimer AM, Silander JA (2009) Effects of an invasive plant species, Celastrus orbiculatus, on soil composition and processes effects of an invasive plant species, Celastrus orbiculatus, on soil composition and processes. Am Midl Nat 161:219–231

    Article  Google Scholar 

  • Leicht-Young SA, Bois ST, Silander JA (2015) Impacts of Celastrus-primed soil on common native and invasive woodland species. Plant Ecol 216:503–516. doi:10.1007/s11258-015-0451-2

    Article  Google Scholar 

  • Levia D, Frost EE (2003) A review and evaluation of stemflow literature in the hydrologic and biogeochemical cycles of forested and agricultural ecosystems. J Hydrol 274:1–29

    CAS  Article  Google Scholar 

  • 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. doi:10.1111/j.1469-8137.2007.02290.x

    CAS  Article  PubMed  Google Scholar 

  • Lin YT, Tang SL, Pai CW, Whitman WB, Coleman DC, Chiu CY (2014) Changes in the soil bacterial communities in a cedar plantation invaded by Moso Bamboo. Microb Ecol 67:421–429. doi:10.1007/s00248-013-0291-3

    Article  PubMed  Google Scholar 

  • Lowe LE (1993) Total and labile acid extractable polysaccharide analysis of soils. In: Carter M (ed) Soil sampling and methods of analysis. Lewis Publishers, Boca Raton, pp 373–376

    Google Scholar 

  • Mattingly KZ, McEwan RW, Paratley RD, Bray SR, Lempke JR, Arthur MA (2016) Recovery of forest floor diversity after removal of the nonnative, invasive plant Euonymus fortunei. J Torrey Bot Soc 143:103–116. doi:10.3159/TORREY-D-14-00051

    Article  Google Scholar 

  • Miller KE, Gorchov DL (2004) The invasive shrub, Lonicera maackii, reduces growth and fecundity of perennial forest herbs. Oecologia 139:359–375. doi:10.1007/s00442-004-1518-2

    Article  PubMed  Google Scholar 

  • Miller WP, Miller DM (1987) A micro-pipette method for soil mechanical analysis. Commun Soil Sci Plant Anal 18:1–15

    CAS  Article  Google Scholar 

  • Muscarella M, Bird K, Larsen M, Placella S, Lennon J (2014) Phosphorus resource heterogeneity in microbial food webs. Aquat Microb Ecol 73:259–272. doi:10.3354/ame01722

    Article  Google Scholar 

  • Oksanen AJ, Blanchet FG, Kindt R, Legendre P, Minchin PR, Hara RBO, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: Community Ecology Package. http://cran.r-project.org/web/packages/vegan/index.html

  • Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44:322–331

    Article  Google Scholar 

  • Osunkoya OO, Bayliss D, Panetta FD, Vivian-Smith G (2010) Leaf trait co-ordination in relation to construction cost, carbon gain and resource-use efficiency in exotic invasive and native woody vine species. Ann Bot 106:371–380. doi:10.1093/aob/mcq119

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Perrett C, Osunkoya OO, Clark C (2012) Cat’s claw creeper vine, Macfadyena unguis-cati (Bignoniaceae), invasion impacts: comparative leaf nutrient content and effects on soil physicochemical properties. Aust J Bot 60:539–548. doi:10.1071/BT12055

    CAS  Article  Google Scholar 

  • Piper CL, Siciliano SD, Winsley T, Lamb EG (2015) Smooth brome invasion increases rare soil bacterial species prevalence, bacterial species richness and evenness. J Ecol 103:386–396. doi:10.1111/1365-2745.12356

    CAS  Article  Google Scholar 

  • Powers JS (2014) Reciprocal interactions between lianas and forest soi. In: Schnitzer SA, Bongers F, Burnham RJ, Putz FE (eds) Ecology of Lianas, 187th edn. Wiley-Blackwell, Chichester, p 175

    Google Scholar 

  • Pysek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand. Biological Invasions. Springer, Berlin, pp 97–126

    Chapter  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. RA Lang Environ Stat Comput

  • Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol Monogr 62:365–392

    Article  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Ecology 94:13730–13734. doi:10.1073/pnas.94.25.13730

    CAS  Google Scholar 

  • Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457. doi:10.1111/j.1469-8137.2006.01715.x

    Article  PubMed  Google Scholar 

  • Roberts DW (2015) Labdsv: ordination and multivariate analysis for ecology. http://cran.r-project.org/web/packages/labdsv/index.html

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. doi:10.1128/AEM.01541-09

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Smith LM, Reynolds HL (2012) Positive plant-soil feedback may drive dominance of a woodland invader, Euonymus fortunei. Plant Ecol 213:853–860. doi:10.1007/s11258-012-0047-z

    Article  Google Scholar 

  • Smith LM, Reynolds HL (2015) Euonymus fortunei dominance over native species may be facilitated by plant–soil feedback. Plant Ecol 216:1401–1406. doi:10.1007/s11258-015-0518-0

    Article  Google Scholar 

  • Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451

    Article  PubMed  Google Scholar 

  • Swearingen J, Slattery B, Reshetiloff K, Zwicker S (2010) Invaders of mid-Atlantic natural areas, 4th edn. U. S Fish and Wlidlife Service, Washington

    Google Scholar 

  • Swedo BL, Glinka C, Rollo DR, Reynolds HL (2008) Soil bacterial community structure under exotic versus native understory forbs in a woodland remnant in Indiana. 117, pp 7–15

  • Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. Blackwell Science Publications, Oxford

    Google Scholar 

  • Tang Y, Kitching RL, Cao M (2012) Lianas as structural parasites: a re-evaluation. Chin Sci Bull 57:307–312. doi:10.1007/s11434-011-4690-x

    Article  Google Scholar 

  • van Soest PJ (1963) Use of detergents in the analysis of fibrous feeds. II. A rapid method for the determination of fiber and lignin. J Assoc Off Anal Chem 46:829–835

    Google Scholar 

  • Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708. doi:10.1111/j.1461-0248.2011.01628.x

    Article  PubMed  Google Scholar 

  • Wharton ME, Barbour RW (1991) Bluegrass land and life. The University of Kentukcy Press, Lexington

    Google Scholar 

  • Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107. doi:10.1023/A:1004347701584

    CAS  Article  Google Scholar 

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Acknowledgements

Milinda Hamilton provided assistance in sample processing; Todd Rounsaville provided access to field sites; Nicolas Body and Kali Mattingly provided field assistance; J.T. Lennon hosted the sabbatical of SRB; and Mario Muscarella provided mothur and R assistance. SRB was supported by the Kenan Sabbatical Support Fund from Transylvania University. This is publication number 16-09-076 of the Kentucky Agricultural Experiment Station and is published with the approval of the Director. This work is supported by the National Institute of Food and Agriculture, U.S. Department of Agriculture, McIntire-Stennis project under accession number 0220128.

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Correspondence to Sarah R. Bray.

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Communicated by Luke Flory.

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Bray, S.R., Hoyt, A.M., Yang, Z. et al. Non-native liana, Euonymus fortunei, associated with increased soil nutrients, unique bacterial communities, and faster decomposition rate. Plant Ecol 218, 329–343 (2017). https://doi.org/10.1007/s11258-016-0689-3

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  • DOI: https://doi.org/10.1007/s11258-016-0689-3

Keywords

  • Invasive species
  • Litter decomposition
  • Soil bacterial community
  • 16S rRNA
  • Legacy effects
  • Wintercreeper