Invasive plants affect soil food webs through various resource inputs including shoot litter, root litter and living root input. The net impact of invasive plants on soil biota has been recognized; however, the relative contributions of different resource input pathways have not been quantified. Through a 2 × 2 × 2 factorial field experiment, a pair of invasive and native plant species (Spartina alterniflora vs. Phragmites australis) was compared to determine the relative impacts of their living roots or shoots and root litter on soil microbial and nematode communities. Living root identity affected bacteria-to-fungi PLFA ratios, abundance of total nematodes, plant-feeding nematodes and omnivorous nematodes. Specifically, the plant-feeding nematodes were 627% less abundant when living roots of invasive S. alterniflora were present than those of native P. australis. Likewise, shoot and root biomass (within soil at 0–10 cm depth) of S. alterniflora was, respectively, 300 and 100% greater than those of P. australis. These findings support the enemy release hypothesis of plant invasion. Root litter identity affected other components of soil microbiota (that is, bacterial-feeding nematodes), which were 34% more abundant in the presence of root litter of P. australis than S. alterniflora. Overall, more variation associated with nematode community structure and function was explained by differences in living roots than root or shoot litter for this pair of plant species sharing a common habitat but contrasting invasion degrees. We conclude that belowground resource input is an important mechanism used by invasive plants to affect ecosystem structure and function.
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Albers D, Schaefer M, Scheu S. 2006. Incorporation of plant carbon into the soil animal food web of an arable system. Ecology 87:235–45.
Andrássy I. 1956. Die rauminhalst and gewichtsbestimmung der fadenwurmer, (Nematoden). Acta Zool Acad Sci Hung 2:1–15.
Bardgett RD, Bowman WD, Kaufmann R, Schmidt SK. 2005. A temporal approach to linking aboveground and belowground ecology. Trends Ecol Evol 20:634–41.
Bardgett RD, Wardle DA. 2010. Aboveground–belowground linkages, biotic interactions, ecosystem processes, and global change. Oxford Series in Ecology and Evolution. New York: Oxford University Press.
Bastow JL, Preisser EL, Strong DR. 2008. Holcus lanatus invasion slows decomposition through its interaction with a macroinvertebrate detritivore, Porcellio scaber. Biol Invasions 10:191–9.
Bird JA, Torn MS. 2006. Fine roots vs. needles: a comparison of 13C and 15N dynamics in a ponderosa pine forest soil. Biogeochemistry 79:361–82.
Bongers T. 1990. The maturity index—an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19.
Bossio DA, Scow KM. 1998. Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–78.
Cheng W, Zhang Q, Coleman DC. 1996. Is available carbon limiting microbial respiration in the rhizosphere? Soil Biol Biochem 28:1283–8.
Chen H, Li B, Fang C, Chen J, Wu J. 2007a. Exotic plant influences soil nematode communities through litter input. Soil Biol Biochem 39:1782–93.
Chen H, Li B, Hu J, Chen J, Wu J. 2007b. Effects of Spartina alterniflora invasion on benthic nematode communities in the Yangtze Estuary. Mar Ecol Prog Ser 336:99–110.
Chen Z, Guo L, Jin B, Wu J, Zheng G. 2009. Effect of the exotic plant Spartina alterniflora on macrobenthos communities in salt marshes of the Yangtze River Estuary, China. Estuar Coast Shelf Sci 82:265–72.
Chen Z, Li B, Chen J. 2004. Ecological consequences and management of Spartina spp. invasions in coastal ecosystems. Biodivers Sci 12:280–9.
Clarke KR, Warwick RM. 1994. Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: Plymouth Marine Laboratory.
Dawson W, Schrama M. 2016. Identifying the role of soil microbes in plant invasions. J Ecol 104:1211–18.
De Deyn GB, Quirk H, Ostle N, Bardgett RD. 2011. Rapid transfer of photosynthetic carbon through the plant-soil system in differently managed species-rich grasslands. Biogeosciences 8:1131–9.
Ehrenfeld JG. 2003. Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–23.
Ehrenfeld JG. 2010. Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80.
Eisenhauer N, Reich PB. 2012. Above- and below-ground plant inputs both fuel soil food webs. Soil Biol Biochem 45:156–60.
Eissfeller V, Beyer F, Valtanen K, Hertel D, Maraun M, Polle A, Scheu S. 2013. Incorporation of plant carbon and microbial nitrogen into the rhizosphere food web of beech and ash. Soil Biol Biochem 62:76–81.
Ferris H. 2010. Form and function: metabolic footprints of nematodes in the soil food web. Eur J Soil Biol 46:97–104.
Ferris H, Sánchez-Moreno S, Brennan EB. 2012. Structure, functions and interguild relationships of the soil nematode assemblage in organic vegetable production. Appl Soil Ecol 61:16–25.
Ferris H. 2013. Nematode body mass, biomass and metabolic footprints. Nemaplex (Nematode-Plant Expert Information System), University of California. http://plpnemweb.ucdavis.edu/nemaplex/Ecology/nematode_weights.htm. Accessed 20 Dec 2013
Freschet GT, Cornwell WK, Wardle DA et al. 2013. Linking litter decomposition of above- and below-ground organs to plant-soil feedbacks worldwide. J Ecol 101:943–52.
Frostegård A, Bååth E. 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65.
Frostegård A, Tunlid A, Bååth E. 2011. Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–5.
Griffiths BS, Boag B, Neilson R, Palmer L. 1990. The use of colloidal silica to extract nematodes from small samples of soil or sediment. Nematologica 36:465–73.
Gratton C, Denno RF. 2005. Restoration of arthropod assemblages in a Spartina salt marsh following removal of the invasive plant Phragmites australis. Restor Ecol 13:358–72.
Högberg P, Nordgren A, Buchmann N et al. 2001. Large-scale forest girdling show that current photosynthesis drives soil respiration. Nature 411:789–92.
Hu N, Li H, Tang Z et al. 2016. Community diversity, structure and carbon footprint of nematode food web following reforestation on degraded Karst soil. Sci Rep 6:28138.
Hodson AK, Ferris H, Hollander AD, Jackson LE. 2014. Nematode food webs associated with native perennial plant species and soil nutrient pools in California riparian oak woodlands. Geoderma 228–229:182–91.
Heiri O, Lotter AF, Lemeke G. 2001. Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. J Paleolimnol 25:101–10.
Hansson K, Kleja DB, Kalbitz K, Larsson H. 2010. Amounts of carbon mineralized and leached as DOC during decomposition of Norway spruce needles and fine roots. Soil Biol Biochem 42:178–85.
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 41:1060–5.
Kourtev PS, Ehrenfeld JG, Häggblom M. 2002. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–66.
Li B, Liao C, Zhang X et al. 2009. Spartina alterniflora invasions in the Yangtze River estuary, China: an overview of current status and ecosystem effects. Ecol Eng 35:511–20.
Liao C, Luo Y, Jiang L et al. 2007. Invasion of Spartina alterniflora enhanced ecosystem carbon and nitrogen stocks in the Yangtze Estuary, China. Ecosystems 10:1351–61.
Liao CZ, Luo YQ, Fang CM, Chen JK, Li B. 2008. Litter pool sizes, decomposition, and nitrogen dynamics in Spartina alterniflora-invaded and native coastal marshlands of the Yangtze Estuary. Oecologia 156:589–600.
McCary MA, Mores R, Farfan MA, Wise DH. 2016. Invasive plants have different effects on trophic structure of green and brown food webs in terrestrial ecosystems: a meta-analysis. Ecol Lett 19:328–35.
Moore JC, Berlow EL, Coleman DC et al. 2004. Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600.
Moore JC, McCann K, de Ruiter PC. 2005. Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiologia 49:499–510.
Morriën E, Duyts H, van der Putten WH. 2012. Effects of native and exotic range-expanding plant species on taxonomic and functional composition of nematodes in the soil food web. Oikos 121:181–90.
Osler GHR, Korycinska A, Cole L. 2006. Differences in litter mass change mite assemblage structure on a deciduous forest floor. Ecography 29:811–18.
Pollierer MM, Langel R, Korner C, Maraun M, Scheu S. 2007. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–36.
Pollierer MM, Dyckmans J, Scheu S, Haubert D. 2012. Carbon flux through fungi and bacteria into the forest soil animal food web as indicated by compound-specific 13C fatty acid analysis. Funct Ecol 26:978–90.
Qing H, Yao Y, Xiao Y, Hu F, Sun Y, Zhou C, An S. 2011. Invasive and native tall forms of Spartina alterniflora respond differently to nitrogen availability. Acta Oecol 37:23–30.
Ramsey PW, Rillig MC, Feris KP, Holben WE, Gannon JE. 2006. Choice of methods for soil microbial community analysis: PLFA maximizes power compared to CLPP and PCR-based approaches. Pedobiologia 50:275–80.
Ravit B, Ehrenfeld JG, Haggblom MM. 2003. A comparison of sediment microbial communities associated with Phragmites australis and Spartina altemiflora in two Brackish wetlands of New Jersey. Estuaries 26:465–74.
Reinhart KO, Callaway RM. 2006. Soil biota and invasive plants. New Phytol 170:445–57.
Reinhart KO, VandeVoort R. 2006. Effect of native and exotic leaf litter on macroinvertebrate communities and decomposition in a western Montana stream. Divers Distrib 12:776–81.
Ritz K, Trudgill DL. 1999. Utility of nematode community analysis as an integrated measure of the functional state of soils: perspectives and challenges. Plant Soil 212:1–11.
Ruf A, Kuzyakov Y, Lopatovskaya O. 2006. Carbon fluxes in soil food webs of increasing complexity revealed by 14C labelling and 13C natural abundance. Soil Biol Biochem 38:2390–400.
Sauvadet M, Chauvat M, Cluzeau D, Maron P-A, Villenave C, Bertrand I. 2016. The dynamics of soil micro-food web structure and functions vary according to litter quality. Soil Biol Biochem 95:262–74.
Scheu S. 2002. The soil food web: structure and perspectives. Eur J Soil Biol 38:11–20.
Steffens C, Helfrich M, Joergensen RG, Eissfeller V, Flessa H. 2015. Translocation of 13C-labeled leaf or root litter carbon of beech (Fagus sylvatica L.) and ash (Fraxinus excelsior L.) during decomposition - A laboratory incubation experiment. Soil Biol Biochem 83:125–37.
van der Putten WH, Yeats GW, Duyts H, Reis CS, Karssen G. 2005. Invasive plants and their escape from root herbivory: a worldwide comparison of the root-feeding nematode communities of the dune grass Ammophila arenaria in natural and introduced ranges. Biol Invasions 7:733–46.
Wang M, Chen J-K, Li B. 2007. Characterization of bacterial community structure and diversity in rhizosphere soils of three plants in rapidly changing salt marshes using 16S rDNA. Pedosphere 17:545–56.
Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van Der Putten WH, Wall DH. 2004. Ecological linkages between above and belowground. Science 304:1629–33.
Wolfe BE, Klironomos JN. 2005. Breaking new ground: soil communities and exotic plant invasions. Bioscience 55:477–87.
Yeates GW. 1999. Effects of plant on nematode community structure. Annu Rev Phytopathol 37:127–49.
Yeates GW, Bongers T, De Goede RGM, Freckman DW, Georgieva SS. 1993. Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315–31.
Zhang X, Guan P, Wang Y et al. 2015. Community composition, diversity and metabolic footprints of soil nematodes in differently-aged temperate forests. Soil Biol Biochem 80:118–26.
Zhao H, Huang G, Ma J, Li Y, Tang L. 2014. Decomposition of aboveground and root litter for three desert herbs: mass loss and dynamics of mineral nutrients. Biol Fertil Soils 50:745–53.
This study was financially supported by National Natural Science Foundation of China (Grant No. 41371258), National Basic Research Program of China (Grant No. 2013CB430404) and Collaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China. We are grateful to Zaichao Yang, Jun Yan, Youzheng Zhang and Hequn Liu for their help in field sampling. We also thank Dr. Shuangshuang Liu for her constructive suggestions to our manuscript.
This study was funded by National Natural Science Foundation of China (Grant No. 41371258), National Basic Research Program of China (Grant No. 2013CB430404) and Collaborative Innovation Center for Biodiversity and Conservation in the Three Parallel Rivers Region of China.
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The authors declare that they have no conflict of interest.
Author Contributions PZ and JHW conceived and designed the study. PZ conducted field research, lab measurements and statistical analyses. PZ, JHW, DN, BL wrote the paper.
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Zhang, P., Neher, D.A., Li, B. et al. The Impacts of Above- and Belowground Plant Input on Soil Microbiota: Invasive Spartina alterniflora Versus Native Phragmites australis . Ecosystems 21, 469–481 (2018). https://doi.org/10.1007/s10021-017-0162-8