Abstract
Soil resource heterogeneity can affect plant growth and competitive ability. However, little is known about how soil resource heterogeneity affects competitive interactions between invasive and native plants. We conducted an experiment with an invasive clonal plant Alternanthera philoxeroides and a coexisting native one Alternanthera sessilis. The experiment was a randomized design with three factors, i.e. two species (A. philoxeroides and A. sessilis), two interspecific competition treatments (with and without) and five soil treatments (three homogeneous treatments and two small-scale heterogeneous treatments consisting of two patches of 10 cm × 15 cm and with different initial planting positions). Irrespective of competition, increasing soil resource availability increased the growth of A. philoxeroides. Increasing soil resource availability also increased the growth of A. sessilis without competition, but had no impact with competition. Irrespective of competition, soil resource heterogeneity increased biomass and ramet production of A. philoxeroides, and such effects were independent of initial planting position. For A. sessilis, however, soil resource heterogeneity only increased ramet production when the initial plant was grown in the low-resource patch without competition. Our results suggest that both high soil resource availability and small-scale soil resource heterogeneity can increase the relative competitive ability of the invasive plant A. philoxeroides when grown with its native congener A. sessilis. These findings may partly explain the invasion success of this clonal species in area with high soil resource availability and heterogeneity caused by e.g. nitrogen deposition, fertilization and disturbance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alpert P, Mooney HA (1996) Resource heterogeneity generated by shrubs and topography on coastal sand dunes. Vegetation 122:83–89. https://doi.org/10.1007/BF00052818
Birch CPD, Hutchings MJ (1994) Exploitation of patchily distributed soil resources by the clonal herb Glechoma hederacea. J Ecol 82:653–664. https://doi.org/10.2307/2261272
Bradley BA, Blumenthal DM, Wilcove DS, Ziska LH (2010) Predicting plant invasions in an era of global change. Trends Ecol Evol 25:310–318. https://doi.org/10.1016/j.tree.2009.12.003
Bremner JM (1996) Methods of soil analysis Part 3-chemical methods. In: Bartels MJ, Bigham JM (eds) Nitrogen-total. Soil Science Society of America Inc, Wisconsin, pp 1085–1121
Broadbent A, Stevens CJ, Peltzer DA, Ostle NJ, Orwin KH (2018) Belowground competition drives invasive plant impact on native species regardless of nitrogen availability. Oecologia 186:577–587. https://doi.org/10.1007/s00442-017-4039-5
Chen D, Ali A, Yong XH, Lin CG, Niu XH, Cai AM, Dong BC, Zhou ZX, Wang YJ, Yu FH (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
Cornelissen JHC, Song YB, Yum FH, Dong D (2014) Plant traits and ecosystem effects of clonality: a new research agenda. Ann Bot 114:369–376. https://doi.org/10.1093/aob/mcu113
Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534. https://doi.org/10.1046/j.1365-2745.2000.00473.x
Dickson TL, Mittelbach GG, Reynolds HL, Gross KL (2014) Height and clonality traits determine plant community responses to fertilization. Ecology 95:2443–2452. https://doi.org/10.1890/13-1875.1
Dong BC, Yu GL, Guo W, Zhang MX, Dong M, Yu FH (2010) How internode length, position and presence of leaves affect survival and growth of Alternanthera philoxeroides after fragmentation? Evol Ecol 24:1447–1461. https://doi.org/10.1007/s10682-010-9390-5
Dong BC, Wang JZ, Liu RH, Zhang MX, Luo FL, Yu FH (2015) Soil heterogeneity affects ramet placement of Hydrocotyle vulgaris. J Plant Ecol 8:91–100. https://doi.org/10.1093/jpe/rtu003
Dugdale TM, Champion PD (2012) Control of alligator weed with herbicides: a review. Plant Prot Q 27:70–82
Eilts JA, Mittelbach GG, Reynolds HL, Gross KL (2011) Resource heterogeneity, soil fertility, and species diversity: effects of clonal species on plant communities. Am Nat 177:574–588. https://doi.org/10.1086/659633
Gallardo B, Clavero M, Sanchez MI, Vila M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol 22:151–163. https://doi.org/10.1111/gcb.13004
Gao Y, Wang D, Xing F, Liu J, Wang L (2014) Combined effects of resource heterogeneity and simulated herbivory on plasticity of clonal integration in a rhizomatous perennial herb. Plant Biol 16:774–782. https://doi.org/10.1111/plb.12122
Gastal F, Lemaire G (2002) N uptake and distribution in crops: an agronomical and ecophysiological perspective. J Exp Bot 53:789–799. https://doi.org/10.1023/A:1019640813676
Gough L, Gross KL, Cleland EE, Clark CM, Collins SL, Fargione JE, Pennings SC, Suding KN (2012) Incorporating clonal growth form clarifies the role of plant height in response to nitrogen addition. Oecologia 169:1053–1062. https://doi.org/10.1007/s00442-012-2264-5
Gross KL, Mittelbach GG (2017) Negative effects of fertilization on grassland species richness are stronger when tall clonal species are present. Folia Geobot 52:401–409. https://doi.org/10.1007/s12224-017-9300-5
Holdredge C, Bertness MD, Von Wettberg E, Silliman BR (2010) Nutrient enrichment enhances hidden differences in phenotype to drive a cryptic plant invasion. Oikos 119:1776–1784. https://doi.org/10.1111/j.1600-0706.2010.18647.x
Holzmueller EJ, Jose S (2009) Invasive plant conundrum: what makes the aliens so successful? J Trop Agric 47:18–29
Huang QQ, Shen YD, Li XX, Li SL, Fan ZW (2016) Invasive Eupatorium catarium and Ageratum conyzoides benefit more than does a common native plant from nutrient addition in both competitive and non-competitive environments. Ecol Res 31:145–152. https://doi.org/10.1007/s11284-015-1323-x
Hulvey KB, Zavaleta ES (2012) Abundance declines of a native forb have nonlinear impacts on grassland invasion resistance. Ecology 93:378–388. https://doi.org/10.2307/23143918
Jackson RB, Caldwell MM (1993) The scale of nutrient heterogeneity around individual plants and its quantification with geostatistics. Ecology 74:612–614. https://doi.org/10.2307/1939320
Kao-Kniffin J, Balser TC (2008) Soil fertility and the impact of exotic invasion on microbial communities in Hawaiian forests. Microb Ecol 56:55–63. https://doi.org/10.1007/s00248-007-9323-1
Keser LH, Dawson W, Song YB, Yu FH, Fischer M, Dong M, van Kleunen M (2014) Invasive clonal plant species have a greater root-foraging plasticity than non-invasive ones. Oecologia 174:1055–1064. https://doi.org/10.1007/s00442-013-2829-y
Klimeš L, Klimešová J, Hendriks R, van Groenendael J (1997) Clonal plant architecture: a comparative analysis of form and function. In: de Kroon H, van Groendahl J (eds) Ecology and evolution of clonal plants. Backhuys, Kerkwerve, pp 1–29
Lambers H, Chapin FS III, Pons TL (2008) Plant physiological ecology, 2nd edn. Springer, New York
Leishman MR, Haslehurst T, Ares A, Baruch Z (2007) Leaf trait relationships of native and invasive plants: community- and global-scale comparisons. New Phytol 176:635–643. https://doi.org/10.1111/j.1469-8137.2007.02189.x
Liang SC, Zhang SM, Yu FH, Dong M (2007) Small-scale spatial cross-correlation between ramet population variables of Potentilla reptans var. sericophylla and soil available phosphorus. Chin J Plant Ecol 31:613–618. https://doi.org/10.17521/cjpe.2007.0078
Lin HF, Alpert P, Wang P, Yu FH (2018) Facilitation of amphibious habit by physiological integration in the clonal, perennial, climbing herb Ipomoea aquatica. Sci Total Environ 618:262–268. https://doi.org/10.1016/j.scitotenv.2017.11.025
Liu YJ, van Kleunen M (2017) Responses of common and rare aliens and natives to nutrient availability and fluctuations. J Ecol 105:1111–1122. https://doi.org/10.1111/1365-2745.12733
Liu L, Alpert P, Dong BC, Li JM, Yu FH (2017a) Combined effects of soil heterogeneity, herbivory and detritivory on growth of the clonal plant Hydrocotyle vulgaris. Plant Soil 421:429–437. https://doi.org/10.1007/s11104-017-3476-6
Liu L, Dong BC, Alpert P, Yu FH (2017b) 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
Liu YJ, Kleunen M, Kudo G (2019) Nitrogen acquisition of Central European herbaceous plants that differ in their global naturalization success. Func Ecol 33:566–575. https://doi.org/10.1111/1365-2435.13288
Liu L, Alpert P, Dong BC, Li JM, Yu FH (2020) Modification by earthworms of effects of soil heterogeneity and root foraging in eight species of grass. Sci Total Environ 708:134941. https://doi.org/10.1016/j.scitotenv.2019.134941
Lowe S, Browne M, Boudelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. The Invasive Species Specialists Group (ISSG), a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN), Aukland, New Zealand
Maestre FT, Reynolds JF (2006) Spatial heterogeneity in soil nutrient supply modulates nutrient and biomass responses to multiple global change drivers in model grassland communities. Glob Change Biol 12:2431–2441. https://doi.org/10.1111/j.1365-2486.2006.01262.x
Mommer L, van Ruijven J, Jansen C, van de Steeg HM, de Kroon H (2012) Interactive effects of nutrient heterogeneity and competition: implications for root foraging theory? Func Ecol 26:66–73. https://doi.org/10.1111/j.1365-2435.2011.01916.x
Pan XY, Geng YP, Sosa A, Zhang W, Li B, Chen JK (2007) Invasive Alternanthera philoxeroides: biology, ecology and management. Acta Phytotaxon Sin 45:884–900. https://doi.org/10.1360/aps06134
Peng YK, Luo FL, Li HL, Yu FH (2013) Growth responses of a rhizomatous herb Bolboschoenus planiculmis to scale and contrast of soil nutrient heterogeneity. Chin J Plant Ecol 37:335–343. https://doi.org/10.3724/SP.J.1258.2013.00033
Peng Y, Yang JX, Zhou XH, Peng PH, Li JJ, Zhang SM, He WM (2019) An invasive population of Solidago canadensis is less sensitive to warming and nitrogen-addition than its native population in an invaded range. Biol Invasions 21:151–162. https://doi.org/10.1007/s10530-018-1812-2
Pyšek P, Jarosik V, Hulme PE, Kuhn I, Wild J, Arianoutsou M, Bacher S, Chiron F, Didziulis V, Essl F, Genovesi P, Gherardi F, Hejda M, Kark S, Lambdon PW, Desprez-Loustau ML, Nentwig W, Pergl J, Poboljsaj K, Rabitsch W, Roques A, Roy DB, Shirley S, Solarz W, Vila M, Winter M (2010) Disentangling the role of environmental and human pressures on biological invasions across Europe. Proc Natl Acad Sci USA 107:12157–12162. https://doi.org/10.1073/pnas.1002314107
Roiloa SR, Alpert P, Tharayil N, Hancock G, Bhowmik PC (2007) Greater capacity for division of labour in clones of Fragaria chiloensis from patchier habitats. J Ecol 95:397–405. https://doi.org/10.1111/j.1365-2745.2007.01216.x
Schumacher E, Kueffer C, Edwards PJ, Dietz H (2009) Influence of light and nutrient conditions on seedling growth of native and invasive trees in the Seychelles. Biol Invasions 11:1941–1954. https://doi.org/10.1007/s10530-008-9371-6
Semchenko M, Zobel K, Heinemeyer A, Hutchings MJ (2008) Foraging for space and avoidance of physical obstructions by plant roots: a comparative study of grasses from contrasting habitats. New Phytol 179:1162–1170. https://doi.org/10.1111/j.1469-8137.2008.02543.x
Song YB, Yu FH, Keser LH, Dawson W, Fischer M, Dong M, van Kleunen M (2013) United we stand, divided we fall: a meta-analysis of experiments on clonal integration and its relationship to invasiveness. Oecologia 171:317–327. https://doi.org/10.1007/s00442-012-2430-9
Song YB, Zhou MY, Dai WH, Jiang D, Li WB, Dong M (2014) Effects of node position on regeneration of stolon fragments in congeneric invasive and native Alternanthera species in China. Plant Spec Biol 29:e93–e100. https://doi.org/10.1111/1442-1984.12034
Stuefer JF (1996) Potential and limitations of current concepts regarding the response of clonal plants to environmental heterogeneity. Vegetation 127:55–70. https://doi.org/10.1007/BF00054847
Uddin MN, Robinson RW (2018) Can nutrient enrichment influence the invasion of Phragmites australis? Sci Total Environ 613–614:1449–1459. https://doi.org/10.1016/j.scitotenv.2017.06.131
van Kleunen M, Dawson W, Essl F, Pergl J, Winter M, Weber E, Kreft H, Weigelt P, Kartesz J, Nishino M, Antonova LA, Barcelona JF, Cabezas FJ, Cardenas D, Cardenas-Toro J, Castano N, Chacon E, Chatelain C, Ebel AL, Figueiredo E, Fuentes N, Groom QJ, Henderson L, Inderjit KA, Masciadri S, Meerman J, Morozova O, Moser D, Nickrent DL, Patzelt A, Pelser PB, Baptiste MP, Poopath M, Schulze M, Seebens H, Shu WS, Thomas J, Velayos M, Wieringa JJ, Pysek P (2015) Global exchange and accumulation of non-native plants. Nature 525:100–103. https://doi.org/10.1038/nature14910
Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson P, Schindler D, Schlesinger W, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750. https://doi.org/10.1890/1051-0761(1997)007[0737:HAOTGN]2.0.CO;2
Wang N, Yu FH, Li PX, He WM, Liu FH, Liu JM, Dong M (2008) Clonal integration affects growth, photosynthetic efficiency and biomass allocation, but not the competitive ability, of the alien invasive Alternanthera philoxeroides under severe stress. Ann Bot 101:671–678. https://doi.org/10.1093/aob/mcn005
Wang N, Yu FH, Li PX, He WM, Liu J, Yu GL, Song YB, Dong M (2009) Clonal integration supports the expansion from terrestrial to aquatic environments of the amphibious stoloniferous herb Alternanthera philoxeroides. Plant Biol 11:483–489. https://doi.org/10.1111/j.1438-8677.2008.00133.x
Wang AO, Jiang XX, Zhang QQ, Zhou J, Li HL, Luo FL, Zhang MX, Yu FH (2015) Nitrogen addition increases intraspecific competition in the invasive wetland plant Alternanthera philoxeroides, but not in its native congener Alternanthera sessilis. Plant Spec Biol 30:176–183. https://doi.org/10.1111/1442-1984.12048
Wang T, Hu J, Miao L, Yu D, Liu C (2016) 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, Muller-Scharer H, van Kleunen M, Cai AM, Zhang P, Yan R, Dong BC, Yu FH (2017) Invasive alien plants benefit more from clonal integration in heterogeneous environments than natives. New Phytol 216:1072–1078. https://doi.org/10.1111/nph.14820
Wang YJ, Chen D, Yan R, Yu FH, van Kleunen M (2019) Invasive alien clonal plants are competitively superior over co-occurring native clonal plants. Perspect Plant Ecol 40:125484. https://doi.org/10.1016/j.ppees.2019.125484
Wijesinghe DK, Hutchings MJ (1999) The effects of environmental heterogeneity on the performance of Glechoma hederacea: the interactions between patch contrast and patch scale. J Ecol 87:860–872. https://doi.org/10.1046/j.1365-2745.1999.00395.x
Wild B, Alves RJE, Bárta J, Čapek P, Gentsch N, Guggenberger G, Hugelius G, Knoltsch A, Kuhry P, Lashchinskiy N, Mikutta R, Palmtag J, Prommer J, Schnecker J, Shibistova O, Takriti M, Urich T, Richter A (2018) Amino acid production exceeds plant nitrogen demand in Siberian tundra. Environ Res Lett 13:034002. https://doi.org/10.1088/1748-9326/aaa4fa
Wilsey B (2002) Clonal plants in a spatially heterogeneous environment: effects of integration on Serengeti grassland response to defoliation and urine-hits from grazing mammals. Plant Ecol 159:15–22. https://doi.org/10.1023/a:1015556816307
Wu H, Ismail M, Ding JQ (2017) Global warming increases the interspecific competitiveness of the invasive plant alligator weed, Alternanthera philoxeroides. Sci Total Environ 575:1415–1422. https://doi.org/10.1016/j.scitotenv.2016.09.226
Xu CY, Zhang WJ, Fu CZ, Lu BR (2003) Genetic diversity of alligator weed in China by RAPD analysis. Biodivers Conserv 12:637–645. https://doi.org/10.1023/A:1022453129662
Yu FH, Wang N, Alpert P, He WM, Dong M (2009) Physiological integration in an introduced, invasive plant increases its spread into experimental communities and modifies their structure. Am J Bot 96:1983–1989. https://doi.org/10.3732/ajb.0800426
Zhang HJ, Chang RY, Guo X, Liang XQ, Wang RQ, Liu J (2017) Shifts in growth and competitive dominance of the invasive plant Alternanthera philoxeroides under different nitrogen and phosphorus supply. Environ Exp Bot 135:118–125. https://doi.org/10.1016/j.envexpbot.2016.12.014
Zhou J, Dong BC, Alpert P, Li HL, Zhang MX, Lei GC, Yu FH (2012) Effects of soil nutrient heterogeneity on intraspecific competition in the invasive, clonal plant Alternanthera philoxeroides. Ann Bot 109:813–818. https://doi.org/10.1093/aob/mcr314
Acknowledgements
We thank Cheng-Fu Wei for assistance with the experiment, and the handling editor and two anonymous reviewers for their insightful comments on an earlier version of the manuscript. This research was supported by the National Key Research and Development Program of China (2017YFC0505903), NSFC (41871077, 31870610). Innovative Transdisciplinary Program "Ecological Restoration Engineering" of the Beijing Municipal Education Commission, and the Ten Thousand Talent Program of Zhejiang Province (2018R52016).
Author information
Authors and Affiliations
Contributions
JQG, FHY, WYY conceived and designed the experiments. WYY and XYZ performed the experiments. JFL, JQG, FHY analyzed the data. JFL, JQG, FHY wrote the manuscript; other authors provided editorial advice.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Brian J. Wilsey.
Rights and permissions
About this article
Cite this article
Liang, JF., Yuan, WY., Gao, JQ. et al. Soil resource heterogeneity competitively favors an invasive clonal plant over a native one. Oecologia 193, 155–165 (2020). https://doi.org/10.1007/s00442-020-04660-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04660-6