Abstract
Purpose
Although it is generally accepted that planting exotic plant species alters metabolic function of soil microbial communities, its temporal dynamic is often ignored when evaluating ecological effects of associated land use changes. To investigate the dynamic impacts of successive Eucalyptus planting on carbon metabolic activities of soil microbial communities, we studied community-level physiological profiles of soil microbial communities in different generations of Eucalyptus plantations.
Materials and methods
We studied community-level physiological profiles of soil microbial communities, using the Biolog™ Ecoplates incubation, in adjacent first (G1), second (G2), third (G3), and fourth (G4) generation Eucalyptus plantations that were, respectively, aged 3, 8, 14, and 19 years in Guangxi province, southern China. We used the ‘space-for-time substitution’ approach to investigate the impact of stand age of exotic Eucalyptus plantations on carbon metabolic diversity and activities of soil microbial communities. For each Eucalyptus plantation generation, three experimental plots were randomly selected. In each plot, one composite soil sample from 0 to 10 cm in depth was obtained for the analyses.
Results and discussion
Single carbon source utilization varied with Eucalyptus plantation stand age. Among preselected 31 carbon sources, utilization of 17 carbon sources changed significantly, which was best described by a quadratic function (ten carbon sources) and an exponential function (seven carbon sources). As a result, cumulative averaged metabolic activity and metabolic diversity of soil microbial communities showed quadratic and exponential changes relative to Eucalyptus plantation stand age. The order of cumulative averaged carbon metabolic activity and metabolic diversity were G1 > G4, G3 > G2 and G1 > G2 > G3, G4 (p < 0.05), respectively. The factors contributing to carbon source utilization structure of soil microbial communities for different stand ages of Eucalyptus plantations were shrub richness, soil organic carbon content, microbial biomass carbon, C-to-N ratio, and N-to-P ratio.
Conclusions
Eucalyptus plantation stand age has inconsistent non-linear impacts on two aspects of soil microbial metabolic function: (1) quadratic impacts on carbon metabolic efficiency and (2) exponential impacts on carbon metabolic diversity. The decreasing carbon metabolic diversity has no significant impact on carbon metabolic efficiency during successive Eucalyptus plantings. The results show that the importance of assessing long-term impacts of land use changes on soil microbial communities from exotic plantations by quantifying multi-aspect non-linear changes on soil microbial metabolic function.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11368-013-0669-3/MediaObjects/11368_2013_669_Fig1_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11368-013-0669-3/MediaObjects/11368_2013_669_Fig2_HTML.gif)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11368-013-0669-3/MediaObjects/11368_2013_669_Fig3_HTML.gif)
Similar content being viewed by others
References
Allen AS, Schlesinger WH (2004) Nutrient limitations to soil microbial biomass and activity in loblolly pine forests. Soil Biol Biochem 36:581–589
Andersson M, Michelsen A, Jensen M, Kjoller A (2004) Tropical savannah woodland: effects of experimental fire on soil microorganisms and soil emissions of carbon dioxide. Soil Biol Biochem 36:849–858
Bao SD (2000) Soil and Agricultural Chemistry Analysis, 3rd edn. China Agriculture Press, Beijing (in Chinese)
Berthrong ST, Schadt CW, Pineiro G, Jackson RB (2009) Afforestation alters the composition of functional genes in soil and biogeochemical processes in South American grasslands. Appl Environ Microbiol 75:6240–6248
Burton J, Chen CR, Xu ZH, Ghadiri H (2010) Soil microbial biomass, activity and community composition in adjacent native and plantation forests of subtropical Australia. J Soils Sediments 10:1267–1277
Campbell CD, Grayston SJ, Hirst DJ (1997) Use of rhizosphere carbon sources in sole carbon source tests to discriminate soil microbial communities. J Microbiol Methods 30:33–41
Chauvat M, Zaitsev AS, Wolters V (2003) Successional changes of Collembola and soil microbiota during forest rotation. Oecologia 137:269–276
Chen CR, Xu ZH, Mathers NJ (2004) Soil carbon pools in adjacent natural and plantation forests of subtropical Australia. Soil Sci Soc Am J 68:282–291
Chen Z, Wang XK, Yao FF, Zheng FX, Feng ZZ (2010) Elevated ozone changed soil microbial community in a rice paddy. Soil Sci Soc Am J 74:829–837
Compton JE, Watrud LS, Porteous LA, DeGrood S (2004) Response of soil microbial biomass and community composition to chronic nitrogen additions at Harvard forest. For Ecol Manage 196:143–158
De Marco A, Gentile AE, Arena C, De Santo AV (2005) Organic matter, nutrient content and biological activity in burned and unburned soils of a Mediterranean maquis area of southern Italy. Int J Wildland Fire 14:365–377
Dooley SR, Treseder KK (2012) The effect of fire on microbial biomass: a meta-analysis of field studies. Biogeochemistry 109:49–61
Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manage 196:159–171
Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359
Gong JR, Ge ZW, An R, Duan QW, You X, Huang YM (2012) Soil respiration in poplar plantations in northern China at different forest ages. Plant Soil 360:109–122
Haack SK, Garchow H, Klug MJ, Forney LJ (1995) Analysis of factors affecting the accuracy, reproducibility, and interpretation of microbial community carbon source utilization patterns. Appl Environ Microbiol 61:1458–1468
Hackett CA, Griffiths BS (1997) Statistical analysis of the time-course of Biolog substrate utilization. J Microbiol Methods 30:63–69
Högberg P, Read DJ (2006) Towards a more plant physiological perspective on soil ecology. Trends Ecol Evol 21:548–554
Iovieno P, Alfani A, Bååth E (2010) Soil microbial community structure and biomass as affected by Pinus pinea plantation in two Mediterranean areas. Appl Soil Ecol 45:56–63
Johnston JM, Crossley DA (2002) Forest ecosystem recovery in the southeast US: soil ecology as an essential component of ecosystem management. For Ecol Manage 155:187–203
Kaufmann K, Christophersen M, Buttler A, Harms H, Hohener P (2004) Microbial community response to petroleum hydrocarbon contamination in the unsaturated zone at the experimental field site Vaerlose, Denmark. FEMS Microbiol Ecol 48:387–399
Langley JA, Hungate BA (2003) Mycorrhizal controls on belowground litter quality. Ecology 84:2302–2312
Lima AMN, Silva IR, Neves JCL, Novais RF, Barros NF, Mendonca ES, Smyth TJ, Moreira MS, Leite FP (2006) Soil organic carbon dynamics following afforestation of degraded pastures with Eucalyptus in southeastern Brazil. For Ecol Manage 235:219–231
Liu ZF, Wu JP, Zhou LX, Lin YB, Fu SL (2012) Tree girdling effect on bacterial substrate utilization pattern depending on stand age and soil microclimate in Eucalyptus plantations. Appl Soil Ecol 54:7–13
Ma XX, Gong W, Hu TX, Wang JY, Li XP, Shi W (2010) Effects of conversion of natural forest and slope farmland to Eucalyptus grandis plantation on soil nutrients. J Sichuan Agric Univ 28:56–60 (in Chinese)
Mitchell RJ, Hester AJ, Campbell CD, Chapman SJ, Cameron CM, Hewison RL, Potts JM (2012) Explaining the variation in the soil microbial community: do vegetation composition and soil chemistry explain the same or different parts of the microbial variation? Plant Soil 351:355–362
Neary DG, Klopatek CC, DeBano LF, Ffolliott PF (1999) Fire effects on belowground sustainability: a review and synthesis. For Ecol Manage 122:51–71
Nilsson MC, Wardle DA (2005) Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Front Ecol Environ 3:421–428
Palese AM, Giovannini G, Lucchesi S, Dumontet S, Perucci P (2004) Effect of fire on soil C, N and microbial biomass. Agronomie 24:47–53
Pickett STA (1989) Space-for-time substitution as an alternative to long-term studies. In: Likens GE (ed) Long-term Studies in Ecology. Springer, Berlin Heidelberg New York, pp 110–135
Preston-Mafham J, Boddy L, Randerson PF (2002) Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles—a critique. FEMS Microbiol Ecol 42:1–14
Sauheitl L, Glaser B, Dippold M, Leiber K, Weigelt A (2010) Amino acid fingerprint of a grassland soil reflects changes in plant species richness. Plant Soil 334:353–363
Sicardi M, Garcia-Prechac F, Frioni L (2004) Soil microbial indicators sensitive to land use conversion from pastures to commercial Eucalyptus grandis (Hill ex Maiden) plantations in Uruguay. Appl Soil Ecol 27:125–133
Stephan A, Meyer AH, Schmid B (2000) Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 88:988–998
Teklay T, Shi Z, Attaeian B, Chang SX (2010) Temperature and substrate effects on C & N mineralization and microbial community function of soils from a hybrid poplar chronosequence. Appl Soil Ecol 46:413–421
Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120
Trofymow JA, Porter GL (1998) Introduction to the coastal forest chronosequence project. In: Trofymow JA, MacKinnon A (eds) Proceedings of a Workshop on Structure, Process, and Diversity in Successional Forests of Coastal British Columbia, Victoria, British Columbia. Northwest Science vol 72. Washington State University Press, Washington, pp 4–8
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 19:703–707
Wang B, Liu G, Xue S (2012) Effect of black locust (Robinia pseudoacacia) on soil chemical and microbiological properties in the eroded hilly area of China’s Loess Plateau. Environ Earth Sci 65:597–607
Winding AK (1994) Fingerprinting bacterial soil communities using Biolog microtitre plates. In: Ritz K, Dighton J, Giller KE (eds) Beyond the Biomass: Compositional and Functional Analysis of Soil Microbial Communities. Wiley, Chichester, pp 85–94
Xu ZH, Chen CR (2006) Fingerprinting global climate change and forest management within rhizosphere carbon and nutrient cycling processes. Environ Sci Pollu R 13:293–298
Xu ZH, Ward S, Chen CR, Blumfield T, Prasolova N, Liu JX (2008) Soil carbon and nutrient pools, microbial properties and gross nitrogen transformations in adjacent natural forest and hoop pine plantations of subtropical Australia. J Soils Sediments 8:99–105
Yan M, Zhang X, Zhou G, Gong J, You X (2011) Temporal and spatial variation in soil respiration of poplar plantations at different developmental stages in Xinjiang, China. J Arid Environ 75:51–57
Yarwood SA, Myrold DD, Hogberg MN (2009) Termination of belowground C allocation by trees alters soil fungal and bacterial communities in a boreal forest. FEMS Microbiol Ecol 70:151–162
Yuan BC, Yue DX (2012) Soil microbial and enzymatic activities across a chronosequence of Chinese pine plantation development on the Loess Plateau of China. Pedosphere 22:1–12
Zheng H, Ouyang ZY, Wang XK, Fang ZG, Zhao TQ, Miao H (2005) Effects of regenerating forest cover on soil microbial communities: a case study in hilly red soil region, Southern China. For Ecol Manage 217(2–3):244–254
Zheng Y, Liu XZ, Zhang LM, Zhou ZF, He JZ (2010) Do land utilization pattern affect methanotrophic communities in a Chinese upland red soil? J Environ Sci 22:1936–1943
Acknowledgments
We gratefully acknowledge the financial support of the Knowledge Innovation Program of the Chinese Academy of Science (grant no. KZCX2-EW-QN406) and the National Natural Science Foundation of China (grant no. 31170425, 40871130). We thank Professor Q. B. Wu, F. Y. Wei, and X. G. Pan for the field research. We also appreciate the anonymous reviewers for their invaluable suggestions and Christina Wong for language editing.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Chengrong Chen
Rights and permissions
About this article
Cite this article
Chen, F., Zheng, H., Zhang, K. et al. Non-linear impacts of Eucalyptus plantation stand age on soil microbial metabolic diversity. J Soils Sediments 13, 887–894 (2013). https://doi.org/10.1007/s11368-013-0669-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-013-0669-3