Abstract
Aims
Small islands of safety, accompanied by clonal integration, could have important impacts on plant performance in stressful environments. Although the effects of environmental heterogeneity and clonal integration on clonal plant growth have been well studied, little attention has been paid to the impacts of islands of safety and the interaction with clonal integration on plant performance in the context of soil contamination.
Methods
We conducted an experiment consisting of two soil treatments (with/without an island of safety, i.e., a patch with uncontaminated soil, located in the middle of cadmium-contaminated soil) and two stolon connection statuses (stolon between the mother ramets and their daughter ramets was either severed or kept connected) using the stoloniferous clonal plant Glechoma longituba.
Results
Overall, the presence of the safe island significantly increased the number of ramets, total mass, leaf mass, and stolon mass of the daughter ramets and the whole clone. Clonal integration significantly decreased the number of ramets, total mass, leaf mass, and stolon mass of mother ramets. The presence of the island of safety enhanced total mass, leaf mass, and stolon mass of the mother ramet in the group with severed stolons and root mass and root to shoot ratio in the group with connected stolons.
Conclusions
Building islands of safety can contribute to daughter ramet growth in a contaminated ecosystem, which suggests assembling smaller safe islands coupled with clonal plants with strong clonal integration may be a promising measure to vegetation restoration in heavy metal contaminated ecosystem.
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Data availability
The data used in this study are available from the corresponding author on reasonable request.
References
Adomako MO, Alpert P, Du D-L, Yu F-H (2020) Effects of clonal integration, nutrients and cadmium on growth of the aquatic macrophyte Pistia stratiotes. J Plant Ecol 13:765–772. https://doi.org/10.1093/jpe/rtaa068
Adomako MO, Xue W, Roiloa S, Zhang Q, Du D-L, Yu F-H (2021) Earthworms modulate impacts of soil heterogeneity on plant growth at different spatial scales. Front Plant Sci 12:735495. https://doi.org/10.3389/fpls.2021.735495
Bao SD (2008) Soil and agricultural chemistry analysis, 3rd edn. Agricultrue Press, Beijing
Caraco T, Kelly CK (1991) On the adaptive value of physiological integration in clonal plants. Ecology 72:81–93
Chen D, Ali A, Yong XH, Lin CG, Niu XH, Cai AM, Dong BC, Zhou ZX, Wang YJ, Yu FH (2019a) 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
Chen D, Xiong H, Lin C-G, He W, Zhang Z-W, Wang H, Wang Y-J (2019b) Clonal integration benefits invasive alien plants under water variability in a native community. J Plant Ecol 12:574–582. https://doi.org/10.1093/jpe/rty050
Cheng S (2003) Effects of heavy metals on plants and resistance mechanisms. Environ Sci Pollut Res 10:256–264. https://doi.org/10.1065/espr2002.11.141.2
Feng Y, Lei W, Gu R, Zhao P, Ni S, Lei N (2020) Differential effects of ammonium and nitrate on growth performance of Glechoma longituba under heterogeneous Cd stress. Phyton-Int J Exp Bot 89:667–679. https://doi.org/10.32604/phyton.2020.010160
Gao FL, Alpert P, Yu FH (2021) Parasitism induces negative effects of physiological integration in a clonal plant. New Phytol 229:585–592. https://doi.org/10.1111/nph.16884
Garcia-Palacios P, Maestre FT, Bardgett RD, De Kroon H (2012) Plant responses to soil heterogeneity and global environmental change. J Ecol 100:1303–1314. https://doi.org/10.1111/j.1365-2745.2012.02014.x
Guo W, Hu Z-H (2012) Effects of stolon severing on the expansion of Alternanthera philoxeroides from terrestrial to contaminated aquatic habitats. Plant Species Biol 27:46–52. https://doi.org/10.1111/j.1442-1984.2011.00335.x
Hatamian M, Nejad AR, Kafi M, Souri MK, Shahbazi K (2019) Growth characteristics of ornamental judas tree (Cercis siliquastrum L.) seedlings under different concentrations of lead and cadmium in irrigation water. Acta Scientiarum Polonorum-Hortorum Cultus 18:87–96. https://doi.org/10.24326/asphc.2019.2.8
Holste EK, Kobe RK (2017) Tree species and soil nutrients drive tropical reforestation more than associations with mycorrhizal fungi. Plant Soil 410:283–297. https://doi.org/10.1007/s11104-016-3013-z
Huang L, Yao S-M, Jin Y, Xue W, Yu F-H (2023) Co-contamination by heavy metal and organic pollutant alters impacts of genotypic richness on soil nutrients. Front Plant Sci 14:1124585. https://doi.org/10.3389/fpls.2023.1124585
Hutchings MJ, John EA (2004) The effects of environmental heterogeneity on root growth and root/shoot partitioning. Ann Bot 94:1–8. https://doi.org/10.1093/aob/mch111
Hutchings MJ, Wijesinghe DK (1997) Patchy habitats, division of labour and growth dividends in clonal plants. TREE 12:390–394. https://doi.org/10.1016/s0169-5347(97)87382-x
Jalloh MA, Chen J, Zhen F, Zhang G (2009) Effect of different N fertilizer forms on antioxidant capacity and grain yield of rice growing under Cd stress. J Hazard Mater 162:1081–1085. https://doi.org/10.1016/j.jhazmat.2008.05.146
Liao M, Yu F, Song M, Zhang S, Zhang J, Dong M (2003) Plasticity in R/S ratio, morphology and fitness-related traits in response to reciprocal patchiness of light and nutrients in the stoloniferous herb, Glechoma longituba L. Acta Oecol 24:231–239. https://doi.org/10.1016/j.actao.2003.07.001
Liu L, Alpert P, Dong B-C, Yu F-H (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
Luo FL, Chen Y, Huang L, Wang A, Zhang MX, Yu FH (2014) Shifting effects of physiological integration on performance of a clonal plant during submergence and de-submergence. Ann Bot 113:1265–1274. https://doi.org/10.1093/aob/mcu057
Luo FL, Xing YP, Wei GW, Li CY, Yu FH (2017) Clonal integration facilitates spread of Paspalum paspaloides from terrestrial to cadmium-contaminated aquatic habitats. Plant Biol 19:859–867. https://doi.org/10.1111/plb.12617
Mallick N, Mohn FH (2003) Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus. Ecotoxicol Environ Saf 55:64–69. https://doi.org/10.1016/s0147-6513(02)00122-7
Nasraoui-Hajaji A, Gharbi F, Ghorbel MH, Gouia H (2010) Cadmium stress effects on photosynthesis and PSII efficiency in tomato grown on NO3− or NH4+ as nitrogen source. Acta Botanica Gallica 157:101–115. https://doi.org/10.1080/12538078.2010.10516192
Parmar P, Kumari N, Sharma V (2013) Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Bot Stud 54:45. https://doi.org/10.1186/1999-3110-54-45
Pauliukonis N, Gough L (2004) Effects of the loss of clonal integration on four sedges that differ in ramet aggregation. Plant Ecol 173:1–15
Qian Y, LuChen D, Li D (2022) Physiological integration improves mock strawberry Duchesnea indica (Andr.) Focke uniformity under heterogeneous saline conditions. Sci Hortic 291:110579. https://doi.org/10.1016/j.scienta.2021.110579
Sethy SK, Ghosh S (2013) Effect of heavy metals on germination of seeds. J Nat Sci Biol Med 4:272–275. https://doi.org/10.4103/0976-9668.116964
Shi XP, Bai YF, Song P, Liu YY, Zhang ZW, Zheng B, Jiang CQ, Wang YJ (2021) Clonal integration and phosphorus management under light heterogeneity facilitate the growth and diversity of understory vegetation and soil fungal communities. Sci Total Environ 767:144322. https://doi.org/10.1016/j.scitotenv.2020.144322
Shukla UC, Murthy RC, Kakkar P (2008) Combined effect of ultraviolet-B radiation and cadmium contamination on nutrient uptake and photosynthetic pigments in Brassica campestris L. seedlings. Environ Toxicol 23:712–719. https://doi.org/10.1002/tox.20378
Song M-H, Yu F-H, Ouyang H, Cao G-M, Xu X-L, Cornelissen JHC (2012) Different inter-annual responses to availability and form of nitrogen explain species coexistence in an alpine meadow community after release from grazing. Glob Chang Biol 18:3100–3111. https://doi.org/10.1111/j.1365-2486.2012.02738.x
Song Y-B, Yu F-H, 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
van Mölken T, Sundelin T, Snetselaar R, Stuefer JF (2011) Highways for internal virus spread: patterns of virus movement in the stoloniferous herb Trifolium repens. Botany 89:573–579. https://doi.org/10.1139/B11-044
Wang N, Yu F-H, Li P-X, He W-M, Liu F-H, Liu J-M, 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 F-H, Li P-X, He W-M, Liu J, Yu G-L, Song Y-B, 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 Y-J, Bai Y-F, Zeng S-Q, Yao B, Wang W, Luo F-L (2016a) Heterogeneous water supply affects growth and benefits of clonal integration between co-existing invasive and native Hydrocotyle species. Sci Rep 6:29420. https://doi.org/10.1038/srep29420
Wang Y-J, Shi X-P, Wu X-J, Meng X-F, Wang P-C, Zhou Z-X, Luo F-L, Yu F-H (2016b) Effects of patch contrast and arrangement on benefits of clonal integration in a rhizomatous clonal plant. Sci Rep 6:35459. https://doi.org/10.1038/srep35459
Wang YJ, Mueller-Schaerer 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 P, Hasnain M, Cahill J, Wu D (2020) The multi-response of root foraging strategy to a neighbor, soil heterogeneity and earthworm. Appl Soil Ecol 155:103684. https://doi.org/10.1016/j.apsoil.2020.103684
Wang J, Xu T, Wang Y, Li G, Abdullah I, Zhong Z, Liu J, Zhu W, Wang L, Wang D, Yu F-H (2021) A meta-analysis of effects of physiological integration in clonal plants under homogeneous vs. heterogeneous environments. Funct Ecol 35:578–589. https://doi.org/10.1111/1365-2435.13732
Xiao R, Zhang M, Yao X, Ma Z, Yu F, Bai J (2016) Heavy metal distribution in different soil aggregate size classes from restored brackish marsh, oil exploitation zone, and tidal mud flat of the Yellow River Delta. J Soils Sediments 16:821–830. https://doi.org/10.1007/s11368-015-1274-4
Xing Y-P, Wei G-W, Luo F-L, Li C-Y, Dong B-C, Ji J-S, Yu F-H (2019) Effects of salinity and clonal integration on the amphibious plant Paspalum paspaloides: growth, photosynthesis and tissue ion regulation. J Plant Ecol 12:45–55. https://doi.org/10.1093/jpe/rtx061
Xu L, Wu X, Zhou Z-F (2016) Effects of physiological integration and fertilization on heavy metal remediation in soil by a clonal grass. Pol J Environ Stud 25:395–404. https://doi.org/10.15244/pjoes/60374
Yao X, Xiao R, Ma Z, Xie Y, Zhang M, Yu F (2016) Distribution and contamination assessment of heavy metals in soils from tidal flat, oil exploitation zone and restored wetland in the Yellow River estuary. Wetlands 36:S153–S165. https://doi.org/10.1007/s13157-015-0637-3
Yao SM, Jin Y, Zhang LM, Lei NF, Xue W, Chen JS, Zhang Q, Yu FH (2021a) Effects of soil nutrient heterogeneity and earthworms on aboveground biomass of experimental plant communities. Phyton-Int J Exp Bot 90:1259–1271. https://doi.org/10.32604/phyton.2021.014968
Yao L, Wang J, Li B, Meng Y, Ma X, Si E, Yang K, Shang X, Wang H (2021b) Influences of heavy metals and salt on seed germination and seedling characteristics of halophyte Halogeton glomeratus. Bull Environ Contam Toxicol 106:545–556. https://doi.org/10.1007/s00128-021-03130-w
Yu F, Dong M, Krusi B (2004) Clonal integration helps Psammochloa villosa survive sand burial in an inland dune. New Phytol 162:697–704. https://doi.org/10.1111/j.1469-8137.2004.01073.x
Yu FH, Wang N, He WM, Chu Y, Dong M (2008) Adaptation of rhizome connections in drylands: increasing tolerance of clones to wind erosion. Ann Bot 102:571–577. https://doi.org/10.1093/aob/mcn119
Zhang W, Yang G, Sun J, Chen J, Zhang Y (2015) Clonal integration enhances the performance of a clonal plant species under soil alkalinity stress. PLoS One 10:e0119942. https://doi.org/10.1371/journal.pone.0119942
Zhang X, Li C, Tie D, Quan J, Yue M, Liu X (2021) Epigenetic memory and growth responses of the clonal plant Glechoma longituba to parental recurrent UV-B stress. Funct Plant Biol 48:827–838. https://doi.org/10.1071/fp20303
Zheng Y, Liu P, Liu J, Zhou C, Wang Q, Feng M, Liu G, Zhu X, Lin K (2022) Pollution characteristics and source analysis of heavy metals in farmland soils around the e-waste dismantling sites in Taizhou City, China. J Agro-Environ Sci 41:1442–1451. https://doi.org/10.11654/jaes.2021-1395
Acknowledgments
This study was supported by the Joint Fund of Zhejiang Provincial Natural Science Foundation (grant LTZ20C030001).
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Si-Mei Yao, Wei Xue and Fei-Hai Yu conceived the ideas and designed the experiment. Si-Mei Yao and Wei Xue prepared the materials, conducted the experiment and collected the data. Li-Li Zheng, Wei Xue and Fei-Hai Yu analyzed the data. Li-Li Zheng wrote the first draft of the manuscript. Fei-Hai Yu reviewed and edited the manuscript and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Zheng, LL., Yao, SM., Xue, W. et al. Small islands of safety promote the performance of a clonal plant in cadmium-contaminated soil. Plant Soil 489, 453–464 (2023). https://doi.org/10.1007/s11104-023-06031-5
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DOI: https://doi.org/10.1007/s11104-023-06031-5