Abstract
Following studies that showed negative effects of species loss on ecosystem functioning, newer studies have started to investigate if similar consequences could result from reductions of genetic diversity within species. We tested the influence of genotypic richness and dissimilarity (plots containing one, three, six or 12 genotypes) in stands of the invasive plant Solidago canadensis in China on the decomposition of its leaf litter and associated soil animals over five monthly time intervals. We found that the logarithm of genotypic richness was positively linearly related to mass loss of C, N and P from the litter and to richness and abundance of soil animals on the litter samples. The mixing proportion of litter from two sites, but not genotypic dissimilarity of mixtures, had additional effects on measured variables. The litter diversity effects on soil animals were particularly strong under the most stressful conditions of hot weather in July: at this time richness and abundance of soil animals were higher in 12-genotype litter mixtures than even in the highest corresponding one-genotype litter. The litter diversity effects on decomposition were in part mediated by soil animals: the abundance of Acarina, when used as covariate in the analysis, fully explained the litter diversity effects on mass loss of N and P. Overall, our study shows that high genotypic richness of S. canadensis leaf litter positively affects richness and abundance of soil animals, which in turn accelerate litter decomposition and P release from litter.
Similar content being viewed by others
References
Allan E, Weisser WW, Fischer M, Schulze E-D, Weigelt A, Roscher C, Baade J, Barnard RL, Beßler H, Buchmann N, Buscot F, Ebeling A, Eisenhauer N, Engels C, Fergus AJF, Gleixner G, Gubsch M, Habekost M, Halle S, Klein AM, König S, Kowalski E, Kreutziger Y, Kertscher I, Kummer V, Kuu A, Lange M, Lauterbach D, Le Roux X, Marquard E, Migunova VD, Milcu A, Müller R, Mwangi P, Niklaus P, Oelmann Y, Petermann JS, Poly F, Rottstock T, Rosenkranz S, Sabais A, Scherber C, Scherer-Lorenzen M, Scheu S, Schmitz M, Schumacher J, Soussana J-F, Steinbeiss S, Temperton V, Tscharntke T, Voigt W, Wilcke W, Wirth C, Schmid B (2013) A comparison of the strength of biodiversity effects across multiple functions. Oecologia 173:223–237
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
Ball BA, Hunter MD, Kominoski JS, Swan CM, Bradford MA (2008) Consequences of non-random species loss for decomposition dynamics: experimental evidence for additive and non-additive effects. J Ecol 96:303–313
Balvanera P, Pfisterer AB, Buchmann N, He J-S, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156
Bardgett RD, Chan KF (1999) Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient uptake in montane grassland ecosystems. Soil Biol Biochem 31:1007–1014
Bernays E, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892
Blair JM, Parmelee RW, Beare MH (1990) Decay rates, nitrogen fluxes, and decomposer communities of single- and mixed-species foliar litter. Ecology 71:1976–1985
Bradford MA, Tordoff GM, Eggers T, Jones TH, Newington JE (2002) Microbiota, fauna, and mesh size interactions in litter decomposition. Oikos 99:317–323
Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992
Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera P, O’Connor MI, Gonzalez A (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592
Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67
Chen T, Liu WL, Zhang CB, Wang J (2012) Effects of Solidago canadensis invasion on dynamics of native plant communities and their mechanisms (in Chinese). J Plant Ecol 36:253–261
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
Cragg RG, Bardgett RD (2001) How changes in soil faunal diversity and composition within a trophic group influence decomposition processes. Soil Biol Biochem 33:2073–2081
Crutsinger GM, Collins MD, Fordyce JA, Gompert Z, Nice CC, Sanders NJ (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968
Crutsinger GM, Reynolds WN, Classen AT, Sanders NJ (2008) Disparate effects of plant genotypic diversity on foliage and litter arthropod communities. Oecologia 158:65–75
Crutsinger GM, Sanders NJ, Classen AT (2009) Comparing intra-and inter-specific effects on litter decomposition in an old-field ecosystem. Basic Appl Ecol 10:535–543
Dong M, Lu J, Zhang W, Chen J, Li B (2006a) Canada goldenrod (Solidago canadensis): an invasive alien weed rapidly spreading in China. Acta Phytotaxon Sin 44:72–85
Dong M, Lu B-R, Zhang H-B, Chen J-K, Li B (2006b) Role of sexual reproduction in the spread of an invasive clonal plant Solidago canadensis revealed using intersimple sequence repeat markers. Plant Species Biol 21:13–18
Egli P, Schmid B (2000) Seasonal dynamics of biomass and nitrogen in canopies of Solidago altissima and effects of a yearly mowing treatment. Acta Oecol 21:63–77
Fan X–X, Shen L, Zhang X, Chen X-Y, Fu C-X (2004) Assessing genetic diversity of Ginkgo biloba L. (Ginkgoaceae) populations from China by RAPD markers. Biochem Genet 42:269–278
Gartner TB, Cardon ZG (2004) Decomposition dynamics in mixed-species leaf litter. Oikos 104:230–246
Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380
Godoy O, Castro-Díez P, van Logtestijn RSP, Cornelissen JHC, Valladares F (2010) Leaf litter traits of invasive species slow down decomposition compared to Spanish natives: a broad phylogenetic comparison. Oecologia 162:781–790
González G, Seastedt TR (2001) Soil fauna and plant litter decomposition in tropical and subalpine forests. Ecology 82:955–964
Hartnett DC, Bazzaz FA (1985) The regulation of leaf, ramet and genet densities in experimental populations of the rhizomatous perennial Solidago canadensis. J Ecol 73:429–443
Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243
Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218
Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality. Nature 448:188–190
Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Högberg P, Huss-Danell K, Joshi J, Jumpponen A, körner C, Leadley PW (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127
Hooper DU, Chapin III FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35
Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’Connor MI (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108
Hoorens B, Aerts R, Stroetenga M (2003) Does initial litter chemistry explain litter mixture effects on decomposition? Oecologia 137:578–586
Hoorens B, Stroetenga M, Aerts R (2010) Litter mixture interactions at the level of plant functional types are additive. Ecosystems 13:90–98
Hughes AR, Stachowicz JJ, Williams SL (2009) Morphological and physiological variation among seagrass (Zostera marina) genotypes. Oecologia 159:725–733
Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732
Institute of Soil Science (1978) Analyses of soil physical and chemical properties. Shanghai Scientific and Technical, Shanghai
Isbell F, Calcagno V, Hector A, Connolly J, Harpole WS, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202
Jousset A, Schmid B, Scheu S, Eisenhauer N (2011) Genotypic richness and dissimilarity opposingly affect ecosystem functioning. Ecol Lett 14:537–545
Knops JMH, Wedin D, Tilman D (2001) Biodiversity and decomposition in experimental grassland ecosystems. Oecologia 126:429–433
Lecerf A, Marie G, Kominoski JS, LeRoy CJ, Bernadet C, Swan CM (2011) Incubation time, functional litter diversity, and habitat characteristics predict litter-mixing effects on decomposition. Ecology 92:160–169
LeRoy CJ, Whitham TG, Wooley SC, Marks JC (2007) Within-species variation in foliar chemistry influences leaf-litter decomposition in a Utah river. J N Am Benthol Soc 26:426–438
Li ZY, Xie Y (2002) Invasive alien species in China. China Forestry Publishing House, Beijing
Loreau M (1998) Separating sampling and other effects in biodiversity experiments. Oikos 82:600–602
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76
Lu J-Z, Weng E-S, Wu X-W, Weber E, Zhao B, Li B (2007) Potential distribution of Solidago canadensis in China. Acta Phytotaxon Sin 45:670–674
Madritch MD, Hunter MD (2002) Phenotypic diversity influences ecosystem functioning in an oak sandhills community. Ecology 83:2084–2090
Madritch MD, Hunter MD (2003) Intraspecific litter diversity and nitrogen deposition affect nutrient dynamics and soil respiration. Oecologia 136:124–128
Madritch MD, Donaldson JR, Lindroth RL (2006) Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9:528–537
McTiernan KB, Ineson P, Coward PA (1997) Respiration and nutrient release from tree leaf litter mixtures. Oikos 78:527–538
Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44:322–331
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Petersen H, Luxton M (1982) A comparative analysis of soil fauna populations and their role in decomposition processes. Oikos 39:287–388
Prescott CE, Zabek LM, Staley CL, Kabzems R (2000) Decomposition of broadleaf and needle litter in forests of British Columbia: influences of litter type, forest type, and litter mixtures. Can J For Res 30:1742–1750
Reich PB, Tilman D, Isbell F, Mueller K, Hobbie SE, Flynn DFB, Eisenhauer N (2012) Impacts of biodiversity loss escalate through time as redundancy fades. Science 336:589–592
Schimel JP, Hättenschwiler S (2007) Nitrogen transfer between decomposing leaves of different N status. Soil Biol Biochem 39:1428–1436
Schläpfer F, Schmid B, Seidl I (1999) Expert estimates about effects of biodiversity on ecosystem processes and services. Oikos 84:346–352
Schmid B (1994) Effects of genetic diversity in experimental stands of Solidago altissima—evidence for the potential role of pathogens as selective agents in plant populations. J Ecol 82:165–175
Schmid B, Bazzaz FA (1990) Plasticity in plant size and architecture in rhizome-derived vs. seed-derived Solidago and Aster. Ecology 71:523–535
Schmid B, Bazzaz FA (1994) Crown construction, leaf dynamics, and carbon gain in two perennials with contrasting architecture. Ecol Monogr 64:177–203
Schmid B, Hector A, Saha P, Loreau M (2008) Biodiversity effects and transgressive overyielding. J Plant Ecol 1:95–102
Schmid B, Balvanera P, Cardinale BJ, Godbold J, Pfisterer AB, Raffaelli D, Solan M, Srivastava DS (2009) Consequences of species loss for ecosystem functioning: meta-analyses of data from biodiversity experiments. In: Naeem S, Bunker DE, Hector A, Loreau M, Perrings C (eds) Biodiversity, ecosystem functioning, and human wellbeing. Oxford University Press, Oxford, pp 14–29
Schneider K, Migge S, Norton RA, Scheu S, Langeld R, Reineking A, Maraun M (2004) Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N). Soil Biol Biochem 36:1769–1774
Schweitzer JA, Bailey JK, Rehill BJ, Martinsen GD, Hart SC, Lindroth RL, Keim P, Whitham TG (2004) Genetically based trait in a dominant tree affects ecosystem processes. Ecol Lett 7:127–134
Schweitzer JA, Bailey JK, Hart SC, Whitham TG (2005a) Nonadditive effects of mixing cottonwood genotypes on litter decomposition and nutrient dynamics. Ecology 86:2834–2840
Schweitzer JA, Bailey JK, Hart SC, Wimp GM, Chapman SK, Whitham TG (2005b) The interaction of plant genotype and herbivory decelerate leaf litter decomposition and alter nutrient dynamics. Oikos 110:133–145
Shanghai Almanac Editorial Board (2009) Shanghai Almanac. Shanghai Zhonghua, China
Shen DW, Li YY, Chen XY (2007) Review of clonal diversity and its effects on ecosystem functioning (in Chinese). J Plant Ecol 31:552–560
Smith VC, Bradford MA (2003) Litter quality impacts on grassland litter decomposition are differently dependent on soil fauna across time. Appl Soil Ecol 24:197–203
Treseder KK, Vitousek PM (2001) Potential ecosystem-level effects of genetic variation among populations of Metrosideros polymorpha from a soil fertility gradient in Hawaii. Oecologia 126:266–275
Wang XY, Shen DW, Jiao J, Xu NN, Yu S, Zhou XF, Shi MM, Chen XY (2012) Genotypic diversity enhances invasive ability of Spartina alterniflora. Mol Ecol 21:2542–2551
Wardle DA, Bonner KI, Nicholson KS (1997) Biodiversity and plant litter: experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 79:247–258
Weber E, Schmid B (1998) Latitudinal population differentiation in two species of Solidago (Asteraceae) introduced into Europe. Am J Bot 85:1110–1121
Wieczorek AM, Geber MA (2002) Microsatellite loci for studies of population differentiation and range expansion in Solidago sempervirens L. (Asteraceae). Mol Ecol Notes 2:554–556
Yin WY, Hu SH, Shen YF, Ning YZ, Sun XD, Wu JH, Zhuge Y, Zhang YM (1998) Pritorical keys to soil animals of China. Science Press, Beijing
Acknowledgments
The experiments comply with the current laws of the country (China) in which the experiments were performed. We thank Xiaogang Wang for nutrient determination, Yaobin Song and Zhiheng Wang for valuable suggestions, Pascal A. Niklaus for help with data analysis and Minyan Cui and Bangquan Gao for help in the field. We also thank the associate editor and two anonymous reviewers for their very helpful comments on earlier versions of the manuscript. This study was supported by the Agricultural Commission of Shanghai (2003-15-3), the Science and Technology Commission of Shanghai (10dz1200703, 2010BAK69B14-2), and the 211 Project of East China Normal University. B. S. was supported by the Swiss National Science Foundation (grant no. 130720).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Tim Seastedt.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wang, XY., Miao, Y., Yu, S. et al. Genotypic diversity of an invasive plant species promotes litter decomposition and associated processes. Oecologia 174, 993–1005 (2014). https://doi.org/10.1007/s00442-013-2816-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-013-2816-3