Abstract
Aims
Environmental heterogeneity can influence biological invasions by altering the interspecific competition between native and invasive species. Soils are a key component of the abiotic environment that can vary in small scales. However, it is not clear how the mechanisms that patch size of soil heterogeneity mediates competition between native and invasive plants.
Methods
We grew invasive Rhus typhina and native Rhus chinensis in intraspecific (two seedlings of the same species per pot) and interspecific competition (one seedling of each of the two species per pot) with three different soil treatments: homogeneous (Ho) and two soil heterogeneous (He1 and He2) treatments. In He1 and He2 treatments, the soil consisted of loam and peat patches but different patch sizes, and in Ho treatment, the soil was a uniform mixture of the two types of soil patches.
Results
We found R. typhina had greater overall performance and belowground investment compared to R. chinensis and outcompeted R. chinensis in the interspecific competition regardless of soil heterogeneity. The strength of interspecific competition increased with increasing soil heterogeneity, such that soil heterogeneity amplified the superiority of R. typhina over R. chinensis. Moreover, R. chinensis were more plastic in phenotype than R. typhina, indicating phenotypic plasticity did not confer advantages to R. typhina over R. chinensis across various soil heterogeneity.
Conclusions
Soil heterogeneity can facilitate the invasion of R. typhina by enhancing the advantages over R. chinensis and altering interspecific competition. Phenotypic divergence rather than plasticity plays an important role in mediating interspecific competition.
Similar content being viewed by others
References
Belote RT, Weltzin JF (2006) Interactions between two co-dominant, invasive plants in the understory of a temperate deciduous forest. Biol Invasions 8:1629–1641. https://doi.org/10.1007/s10530-005-3932-8
Bradshaw AD (2006) Unravelling phenotypic plasticity – why should we bother? New Phytol 170:644–648. https://doi.org/10.1111/j.1469-8137.2006.01761.x
Bremner JM (1960) Determination of nitrogen in soil by the Kjeldahl method. J Agr Sci 55:11–33. https://doi.org/10.1017/S0021859600021572
Chamberlain SA, Bronstein JL, Rudgers JA (2014) How context dependent are species interactions? Ecol Lett 17:881–890. https://doi.org/10.1111/ele.12279
Chen B-M, Su J-Q, Liao H-X, Peng S-L (2018) A greater foraging scale, not a higher foraging precision, may facilitate invasion by exotic plants in nutrient-heterogeneous conditions. Ann Bot 121:561–569. https://doi.org/10.1093/aob/mcx172
Chen D, Ali A, Yong X-H, Lin C-G, Niu X-H, Cai A-M, Dong B-C, Zhou Z-X, Wang Y-J, Yu F-H (2019) A multi-species comparison of selective placement patterns of ramets in invasive alien and native clonal plants to light, soil nutrient and water heterogeneity. Sci Total Environ 657:1568–1577. https://doi.org/10.1016/j.scitotenv.2018.12.099
Cuda J, Skalova H, Janovsky Z, Pysek P (2015) Competition among native and invasive Impatiens species: the roles of environmental factors, population density and life stage. AoB Plants 7. https://doi.org/10.1093/aobpla/plv033
Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol Lett 14: 419–431. https://doi.org/10.1111/j.1461-0248.2011.01596.x
Dawson W, Rohr RP, van Kleunen M, Fischer M (2012) Alien plant species with a wider global distribution are better able to capitalize on increased resource availability. New Phytol 194:859–867. https://doi.org/10.1111/j.1469-8137.2012.04104.x
Day KJ, John EA, Hutchings MJ (2003) The effects of spatially heterogeneous nutrient supply on yield, intensity of competition and root placement patterns in Briza media and Festuca ovina. Funct Ecol 17:454–463. https://doi.org/10.1046/j.1365-2435.2003.00758.x
del Pino GA, Brandt AJ, Burns JH (2015) Light heterogeneity interacts with plant-induced soil heterogeneity to affect plant trait expression. Plant Ecol 216:439–450. https://doi.org/10.1007/s11258-015-0448-x
Divíšek J, Chytrý M, Beckage B, Gotelli NJ, Lososová Z, Pyšek P, Richardson DM, Molofsky J (2018) Similarity of introduced plant species to native ones facilitates naturalization, but differences enhance invasion success. Nat Commun 9:4631. https://doi.org/10.1038/s41467-018-06995-4
Fransen B, de Kroon H, Berendse F (2001) Soil nutrient heterogeneity alters competition between two perennial grass species. Ecology 82:2534–2546. https://doi.org/10.1890/0012-9658(2001)082[2534:SNHACB]2.0.CO;2
Funk JL (2008) Differences in plasticity between invasive and native plants from a low resource environment. J Ecol 96:1162–1173. https://doi.org/10.1111/j.1365-2745.2008.01435.x
Gao Y, Xing F, Jin Y, Nie D, Wang Y (2012) Foraging responses of clonal plants to multi-patch environmental heterogeneity: spatial preference and temporal reversibility. Plant Soil 359:137–147. https://doi.org/10.1007/s11104-012-1148-0
Gao Y, Yu H-W, He W-M (2014) Soil space and nutrients differentially promote the growth and competitive advantages of two invasive plants. J Plant Ecol 7:396–402. https://doi.org/10.1093/jpe/rtt050
Gao FL, He QS, Zhang YD, Hou JH, Yu FH (2021) Effects of soil nutrient heterogeneity on the growth and invasion success of alien plants: a multi-species study. Front Eco Evol 8. https://doi.org/10.3389/fevo.2020.619861
Godoy O, Valladares F, Castro-Díez P (2011) Multispecies comparison reveals that invasive and native plants differ in their traits but not in their plasticity. Funct Ecol 25:1248–1259. https://doi.org/10.1111/j.1365-2435.2011.01886.x
Grace JB (1995) On the measurement of plant competition intensity. Ecology 76:305–308. https://doi.org/10.2307/1940651
Gruntman M, Groß D, Májeková M, Tielbörger K (2017) Decision-making in plants under competition. Nat Commun 8:2235. https://doi.org/10.1038/s41467-017-02147-2
Guo X, Xu ZW, Li MY, Ren XH, Liu J, Guo WH (2020) Increased soil moisture aggravated the competitive effects of the invasive tree Rhus typhina on the native tree Cotinus coggygria. BMC Ecol 20:17. https://doi.org/10.1186/s12898-020-00284-9
Guo Q, Cade BS, Dawson W, Essl F, Kreft H, Pergl J, van Kleunen M, Weigelt P, Winter M, Pyšek P (2021) Latitudinal patterns of alien plant invasions. J Biogeogr 48:253–262. https://doi.org/10.1111/jbi.13943
Hiatt D, Flory SL (2020) Populations of a widespread invader and co-occurring native species vary in phenotypic plasticity. New Phytol 225:584–594. https://doi.org/10.1111/nph.16225
Hodge A (2004) The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol 162:9–24. https://doi.org/10.1111/j.1469-8137.2004.01015.x
Hutchings MJ, de Kroon H (1994) Foraging in plants: the role of morphological plasticity in resource acquisition. In: Begon M, Fitter AH (eds) Advances in ecological research. Academic Press, Cambridge
Hutchings MJ, John EA, Wijesinghe DK (2003) Toward understanding the consequences of soil heterogeneity for plant populations and communities. Ecology 84:2322–2334. https://doi.org/10.1890/02-0290
Keser LH, Visser EJW, Dawson W, Song Y-B, Yu F-H, Fischer M, Dong M, van Kleunen M (2015) Herbaceous plant species invading natural areas tend to have stronger adaptive root foraging than other naturalized species. Front Plant Sci 6. https://doi.org/10.3389/fpls.2015.00273
Liang JF, Yuan WY, Gao JQ, Roiloa SR, Song MH, Zhang XY, Yu FH (2020) Soil resource heterogeneity competitively favors an invasive clonal plant over a native one. Oecologia 193:155–165. https://doi.org/10.1007/s00442-020-04660-6
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc T 11:591–592. https://doi.org/10.1042/bst0110591
Liu L, Dong B-C, Alpert P, Yu F-H (2017) Effects of soil substrate heterogeneity and moisture on interspecific competition between Alternanthera philoxeroides and four native species. J Plant Ecol 10:528–537. https://doi.org/10.1093/jpe/rtw052
Luo YJ, Guo WH, Yuan YF, Liu J, Du N, Wang RQ (2014) Increased nitrogen deposition alleviated the competitive effects of the introduced invasive plant Robinia pseudoacacia on the native tree Quercus acutissima. Plant Soil 385:63–75. https://doi.org/10.1007/s11104-014-2227-1
Marchini GL, Maraist CA, Cruzan MB (2019) Trait divergence, not plasticity, determines the success of a newly invasive plant. Ann Bot 123:667–679. https://doi.org/10.1093/aob/mcy200
Matzek V (2012) Trait values, not trait plasticity, best explain invasive species' performance in a changing environment. PLoS One 7:e48821. https://doi.org/10.1371/journal.pone.0048821
Melbourne BA, Cornell HV, Davies KF, Dugaw CJ, Elmendorf S, Freestone AL, Hall RJ, Harrison S, Hastings A, Holland M, Holyoak M, Lambrinos J, Moore K, Yokomizo H (2007) Invasion in a heterogeneous world: resistance, coexistence or hostile takeover? Ecol Lett 10:77–94. https://doi.org/10.1111/j.1461-0248.2006.00987.x
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2020) Vegan: community ecology package
Ordonez A, Wright IJ, Olff H (2010) Functional differences between native and alien species: a global-scale comparison. Funct Ecol 24:1353–1361. https://doi.org/10.1111/j.1365-2435.2010.01739.x
Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367. https://doi.org/10.1242/jeb.02070
Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2020) Nlme: linear and nonlinear mixed effects models
Price J, Tamme R, Gazol A, de Bello F, Takkis K, Uria-Diez J, Kasari L, Pärtel M, Michalet R (2017) Within-community environmental variability drives trait variability in species-rich grasslands. J Veg Sci 28:303–312. https://doi.org/10.1111/jvs.12487
R Development Core Team (2019) R: a language and environment for statistical computing. Version 3.6.1. R Foundation for Statistical Computing. http://www.R-project.org
Roiloa SR, Sánchez-Rodríguez P, Retuerto R (2014) Heterogeneous distribution of soil nutrients increase intra-specific competition in the clonal plant Glechoma hederacea. Plant Ecol 215:863–873. https://doi.org/10.1007/s11258-014-0338-7
Sax DF, Brown JH (2000) The paradox of invasion. Glob Ecol Biogeogr 9:363–371. https://doi.org/10.1046/j.1365-2699.2000.00217.x
Stark J, Lehman R, Crawford L, Enquist BJ, Blonder B (2017) Does environmental heterogeneity drive functional trait variation? A test in montane and alpine meadows. Oikos 126:1650–1659. https://doi.org/10.1111/oik.04311
Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol Lett 17:866–880. https://doi.org/10.1111/ele.12277
Tamme R, Gazol A, Price JN, Hiiesalu I, Pärtel M (2016) Co-occurring grassland species vary in their responses to fine-scale soil heterogeneity. J Veg Sci 27:1012–1022. https://doi.org/10.1111/jvs.12431
Tan XF, Guo X, Guo WH, Liu SN, Du N (2018) Invasive Rhus typhina invests more in height growth and traits associated with light acquisition than do native and non-invasive alien shrub species. Trees 32:1103–1112. https://doi.org/10.1007/s00468-018-1698-8
Valladares F, Sanchez-Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116. https://doi.org/10.1111/j.1365-2745.2006.01176.x
van Kleunen M, Weber E, Fischer M (2010) A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett 13:235–245. https://doi.org/10.1111/j.1461-0248.2009.01418.x
Vilà M, Williamson M, Lonsdale M (2004) Competition experiments on alien weeds with crops: lessons for measuring plant invasion impact? Biol Invasions 6:59–69. https://doi.org/10.1023/B:BINV.0000010122.77024.8a
Wang GM, Jiang GM, Yu SL, Li YH, Liu H (2008) Invasion possibility and potential effects of Rhus typhina on Beijing municipality. J Integr Plant Biol 50:522–530. https://doi.org/10.1111/j.1744-7909.2008.00660.x
Wang T, Hu JT, Miao LL, Yu D, Liu CH (2016a) The invasive stoloniferous clonal plant Alternanthera philoxeroides outperforms its co-occurring non-invasive functional counterparts in heterogeneous soil environments - invasion implications. Sci Rep 6:38036. https://doi.org/10.1038/srep38036
Wang YJ, Shi XP, Meng XF, Wu XJ, Luo FL, Yu FH (2016b) Effects of spatial patch arrangement and scale of Covarying resources on growth and intraspecific competition of a clonal plant. Front Plant Sci 7:753. https://doi.org/10.3389/fpls.2016.00753
Weber E, Gut D (2004) Assessing the risk of potentially invasive plant species in Central Europe. J Nat Conserv 12:171–179. https://doi.org/10.1016/j.jnc.2004.04.002
Wei W, Zhu P, Chen PD, Huang QQ, Bai XF, Ni GY, Hou YP (2020) Mixed evidence for plant–soil feedbacks in forest invasions. Oecologia 193:665–676. https://doi.org/10.1007/s00442-020-04703-y
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827. https://doi.org/10.1038/nature02403
Xue W, Bezemer TM, Berendse F (2019) Soil heterogeneity and plant species diversity in experimental grassland communities: contrasting effects of soil nutrients and pH at different spatial scales. Plant Soil 442:497–509. https://doi.org/10.1007/s11104-019-04208-5
Yuan YF, Guo WH, Ding WJ, Du N, Luo YJ, Liu J, Xu F, Wang RQ (2013) Competitive interaction between the exotic plant Rhus typhina L. and the native tree Quercus acutissima Carr. in Northern China under different soil N:P ratios. Plant Soil 372:389–400. https://doi.org/10.1007/s11104-013-1748-3
Zhang R, Zhou ZC, Luo WJ, Wang Y, Feng ZP (2013) Effects of nitrogen deposition on growth and phosphate efficiency of Schima superba of different provenances grown in phosphorus-barren soil. Plant Soil 370:435–445. https://doi.org/10.1007/s11104-013-1644-x
Zheng Y-L, Feng Y-L, Zhang L-K, Callaway RM, Valiente-Banuet A, Luo D-Q, Liao Z-Y, Lei Y-B, Barclay GF, Silva-Pereyra C (2015) Integrating novel chemical weapons and evolutionarily increased competitive ability in success of a tropical invader. New Phytol 205:1350–1359. https://doi.org/10.1111/nph.13135
Zhou C, Huang M, Ren H, Yu J, Wu J, Ma X (2017) Bioaccumulation and detoxification mechanisms for lead uptake identified in Rhus chinensis mill. Seedlings. Ecotoxicol Environ Saf 142:59–68. https://doi.org/10.1016/j.ecoenv.2017.03.052
Acknowledgements
We are grateful to Hui Wang for her help during the experiment.
Funding
The research was supported by the National Natural Science Foundation of China (Nos. 31500264, 31970347, 31971718), the Natural Science Foundation of Shandong Province, China (No. ZR2019BC083) and the Qingdao Agricultural University Doctoral Start-Up Fund (Nos. 6631115021, 6631120094).
Author information
Authors and Affiliations
Contributions
Xiao Guo conceived and designed the experiments. Zhong-Yi Zhang carried out the experiment and data collection. Yi Hu, Zhen-Wei Xu and Ming-Yan Li analyzed the data and wrote the draft manuscript. All authors contributed to the editing and revising of the final version of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Janusz J. Zwiazek.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 455 kb)
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Hu, Y., Xu, ZW., Li, MY. et al. Increasing soil heterogeneity strengthens the inhibition of a native woody plant by an invasive congener. Plant Soil 481, 677–690 (2022). https://doi.org/10.1007/s11104-022-05666-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05666-0