Abstract
Exotic plant invasions into Hawaiian montane forests have altered many important nutrient cycling processes and pools. Across different ecosystems, researchers are uncovering the mechanisms involved in how invasive plants impact the soil microbial community—the primary mediator of soil nutrient cycling. We examined whether the invasive plant, Hedychium gardnerianum, altered microbial community composition in forests dominated by a native tree, Metrosideros polymorpha, under varying soil nutrient limitations and soil fertility properties within forest plots of the Hawaii long-term substrate age gradient (LSAG). Microbial community lipid analysis revealed that when nutrient limitation (as determined by aboveground net primary production [ANPP]) and soil fertility were taken into account, plant species differentially altered soil microbial community composition. Microbial community characteristics differed under invasive and native plants primarily when N or P was added to the older, highly weathered, P-limited soils. Long-term fertilization with N or P at the P-limited site led to a significant increase in the relative abundance of the saprophytic fungal indicator (18:2ω6c,9c) under the invasive plant. In the younger, N-limited soils, plant species played a minor role in influencing soil microbial community composition. We found that the general rhizosphere microbial community structure was determined more by soil fertility than by plant species. This study indicates that although the aggressive invasion of a nutrient-demanding, rapidly decomposable, and invasive plant into Hawaiian forests had large impacts on soil microbial decomposers, relatively little impact occurred on the overall soil microbial community structure. Instead, soil nutrient conditions were more important determinants of the overall microbial community structure within Hawaii’s montane forests.
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 141: 612–619
Arao, T (1999) In situ detection of changes in soil bacterial and fungal activities by measuring 13C incorporation into soil phospholipid fatty acids from 13C acetate. Soil Biol Biochem 31: 1015–1020
Asner, GP, Vitousek, PM (2005) Remote analysis of biological invasion and biogeochemical change. Proc Natl Acad Sci U S A 102: 4383–4386
Bååth, E, Anderson, TH (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35: 955–963
Balser, TC, McMahon, K, Bart, D, Bronson, D, Coyle, D, Craig, N, Flores, M, Forshay, K, Jones, S, Kent, A, Shade, A (2006) Bridging the gap between micro- and macroscale perspectives on ecosystem response to disturbance. Plant Soil 289: 59–70
Balser, TC (2005) Humification. In: Hillel, D, Hatfield, J, Powlson, D, Rosenzweig, C (Eds.) Encyclopedia of Soils in the Environment, Vol. 2, Elsevier, Oxford, UK, pp 195–207
Balser, TC, Firestone, MK (2005) Linking microbial community composition and soil processes in a California annual grassland and mixed-conifer forest. Biogeochemistry 73: 395–415
Balser, TC (2002) The impact of long-term nitrogen addition on microbial community composition in three Hawaiian forest soils. In: Galloway, J, Cowling, E, Erisman, JW, Wisniewski, J, Jordan, C (Eds.) Optimizing Nitrogen Management in Food and Energy Production and Environmental Protection, Swets and Zeitlinger B.V., Lisse, pp 500–504
Belnap, J, Phillips, SL (2001) Soil biota in an ungrazed grassland: response to annual grass (Bromus tectorum) invasion. Ecol Appl 11: 1261–1275
Bever, JD, Westover, KM, Antonovics, J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85: 561–573
Bligh, EG, Dyer, WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37: 911–917
Bradley, K, Drijber, RA, Knops, J (2006) Increased N availability in grassland soils modifies their microbial communities and decreases the abundance of arbuscular mycorrhizal fungi. Soil Biol Biochem 38: 1583–1595
Callaway, RM, Thelen, GC, Rodriguez, A, Holben, WH (2004) Soil biota and exotic plant invasion. Science 427: 731–733
Carney, KM, Matson, PA (2006) The influence of tropical plant diversity and composition on soil microbial communities. Microb Ecol 52: 226–238
Crews, TE, Kitayama, K, Fownes, JH, Riley, RH, Herbert, DA, Mueller-Dombois, D, Vitousek, PM (1995) Changes in soil phosphorus fractions and ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76: 1407–1424
Ehrenfeld, JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6: 503–523
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
Ehrenfeld, JG, Scott, N (2001) Invasive species and the soil: effects on organisms and ecosystem processes. Ecol Appl 11: 1259–1260
Evans, RD, Rimer, R, Sperry, L, Belnap, J (2001) Exotic plant invasion alters nitrogen dynamics in an arid grassland. Ecol Appl 11: 1301–1310
Fisk, MC, Fahey, TJ (2001) Microbial biomass and nitrogen cycling responses to fertilization and litter removal in young northern hardwood forests. Biogeochemistry 53: 201–223
Fraterrigo, JM, Balser, TC, Turner, MG (2006) Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 87: 570–579
Funk, JL (2005) Hedychium gardnerianum invasion into Hawaiian montane rainforest: interactions among litter quality, decomposition rate, and soil nitrogen availability. Biogeochemistry 76: 441–451
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
Hedin, LO, Vitousek, PM, Matson, PA (2003) Nutrient losses over four million years of tropical forest development. Ecology 84: 2231–2255
Herbert, DA, Fownes, JH (1995) Phosphorus limitation of forest leaf-area and net primary production on a highly weathered soil. Biogeochemistry 29: 223–235
Kao-Kniffin, JT, Balser, TC (2007) Elevated CO2 differentially alters belowground plant and soil microbial community structure in reed canary grass-invaded experimental wetlands. Soil Biol Biochem 39: 517–525
Kourtev, PS, Ehrenfeld, JG, Haggblom, M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35: 895–905
Kourtev, PS, Ehrenfeld, JG, Haggblom, M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83: 3152–3166
Levine, JM, Montserrat, V, D’Antonio, CM, Dukes, JS, Grigulis, K, Lavorel, S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B 270: 775–781
Mack, MC, D’Antonio, CM (2003) Exotic grasses alter controls over soil nitrogen dynamics in a Hawaiian woodland. Ecol Appl 13: 154–166
Marilley, L, Aragno, M (1999) Phylogenetic diversity of bacterial communities differing in degree of proximity of Lolium perenne and Trifolium repens roots. Appl Soil Ecol 13: 127–136
Meyerson, LA, Saltonstall, K, Windham, L, Kiviat, E, Findlay, S (2000) A comparison of Phragmites australis in freshwater and brackish Marsh environments in North America. Wetlands Ecol Manag 8: 89–103
Ostertag, R, Verville, JH (2002) Fertilization with nitrogen and phosphorus increases abundance of non-native species in Hawaiian montane forests. Plant Ecol 162: 77–90
Otto, S, Groffman, PM, Findlay, SEG, Arreola, AE (1999) Invasive plant species and microbial processes in a tidal freshwater marsh. J Environ Qual 28: 1252–1257
Pennanen, T, Liski, J, Bååth, E, Kitunen, V, Uotila, J, Westman, CJ, Fritze, H (1999) Structure of the microbial communities in coniferous forest soils in relation to site fertility and stand development stage. Microb Ecol 38: 168–179
Reinhart, KO, Callaway, RM (2006) Soil biota and invasive plants. New Phytol 170: 445–457
Richardson, SJ, Peltzer, DA, Allen, RB, McGlone, MS, Parfitt, RL (2004) Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139: 267–276
Schimel, J, Balser, TC, Wallenstein, M (2007) Stress effects on microbial communities and the implications for ecosystem function. Ecology (in press)
Schmidt SK, Lipson, DA, Ley, RE, Fisk, MC, West, AE (2004) Impacts of chronic nitrogen additions vary seasonally and by microbial functional group in tundra soils. Biogeochemistry 69: 1–17
Schlegel, HG (1992) General Microbiology. Cambridge University Press, Cambridge, 655 pp
Steenwerth, KL, Jackson, LE, Calderón, FJ, Stromberg, MR, Scow, KM (2003) Soil microbial community composition and land use history in cultivated and grassland ecosystems of coastal California. Soil Biol Biochem 35: 489–500
Steer, J, Harris, JA (2000) Shifts in the microbial community in the rhizosphere and non-rhizosphere soils during the growth of Agrostis stolonifera. Soil Biol Biochem 32: 869–878
Smithwick, EAH, Turner, MG, Metzger, KL, Balser, TC (2005) Variation in \( {\text{NH}}^{{\text{ + }}}_{{\text{4}}} \) mineralization and microbial communities with stand age in lodgepole pine (Pinus contorta) forests, Yellowstone National Park (USA). Soil Biol Biochem 37: 1546–1559
Tscherko, D, Hammesfahr, U, Marx, MC, Kandeler, E (2004) Shifts in rhizosphere microbial communities and enzyme activity of Poa alpina across an alpine chronosequence. Soil Biol Biochem 36: 1685–1698
Vitousek, PM, Farrington, H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37: 63–75
Vitousek, PM, Walker, LR, Whiteaker, LD, Mueller-Dombois, D, Matson, PA (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238: 802–804
Wester, L (1992) Origin and distribution of adventive alien flowering plants in Hawaii. In: Stone, CP, Smith, CW, Tunison, JP (Eds.) Alien Plant Invasions in Native Ecosystems of Hawaii: Management and Research, Cooperative National Park Resources Studies Unit/University of Hawaii at Manoa, Honolulu, pp 99–154
White, DC, Ringelberg, DB (1998) Signature lipid biomarker analysis. In: Burlage, RS, Atlas, R, Stahl, D, Geesey, G, Sayler, G (Eds.) Techniques in Microbial Ecology, Oxford University Press, New York, pp 255–273
Williamson, WA, Wardle, DA, Yeates, GW (2005) Changes in soil microbial and nematode communities during ecosystem decline across a long-term chronosequence. Soil Biol Biochem 37: 1289–1301
Acknowledgments
We thank Peter Vitousek for the use of his long-term fertilization plots on Kauai and Hawaii. We also thank Heraldo Farrington for the help in the field and Harry Read for the assistance with lipid analysis. This research was funded by the Andrew W. Mellon Foundation and the University of Wisconsin–Madison Graduate School.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kao-Kniffin, J., Balser, T.C. Soil Fertility and the Impact of Exotic Invasion on Microbial Communities in Hawaiian Forests. Microb Ecol 56, 55–63 (2008). https://doi.org/10.1007/s00248-007-9323-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-007-9323-1