Skip to main content
SpringerLink
Log in

Copper tolerant Elsholtzia splendens facilitates Commelina communis on a copper mine spoil

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

There is evidence that plant facilitation occurs in heavy metal wastelands, but the extent and mechanisms of facilitation are not known. The copper (Cu) tolerant Elsholtzia splendens is a dominant pioneer species during the secondary succession on copper mine spoils in eastern China. Species appearing later are often associated with patches of E. splendens. We hypothesize that E. splendens facilitates neighbors by modifying local soil properties.

Methods

We conducted a field study on a heavy metal wasteland with local variation in soil Cu level to investigate the performance of a target species, Commelina communis, growing in open gaps vs. growing with E. splendens. Soil physicochemical and biological properties, biomass, plant interaction intensity as well as heavy metal concentration in C. communis were measured to study the effects of the presence of E. splendens.

Results

Effects of the presence of E. splendens on C. communis were generally positive, but negative effects were sometimes observed. Positive effects of E. splendens increased with increasing soil Cu level. Soil microbial activity was higher in the presence of E. splendens. Our results are consistent with the hypothesis that facilitation occurred through enrichment of the microbial properties of the soil, especially soil respiration rate and enzyme activity.

Conclusions

Our study highlights the importance of soil-mediated plant-plant interactions for the establishment of C. communis on heavy metal-contaminated sites. These interactions are important for the restoration of heavy metal wastelands.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alef K (1995) Estimation of soil respiration. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic, London, pp 464–467

    Google Scholar 

  • Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686

    Article  Google Scholar 

  • Blair GJ, Lefroy RDB, Lisle L (1995) Soil carbon fractions based on their degree of oxidation and the development of a carbon management index for agricultural systems. Aust J Agric Res 46:1459–1466

    Article  Google Scholar 

  • Bowker MA, Soliveres S, Maestre FT (2010) Competition increases with abiotic stress and regulates the diversity of biological soil crusts. J Ecol 98:551–560

    Article  Google Scholar 

  • Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G, Liancourt P, Tielbörger K, Travis JMJ, Anthelme F, Armas C, Coll L, Corcket E, Delzon S, Forey E, Kikvidze Z, Olofsson J, Pugnaire F, Quiroz CL, Saccone P, Schiffers K, Seifan M, Touzard B, Michalet R (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34

    Article  Google Scholar 

  • Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125

    Article  Google Scholar 

  • Butterfield BJ (2009) Effects of facilitation on community stability and dynamics: synthesis and future directions. J Ecol 97:1192–1201

    Article  Google Scholar 

  • Callaway RM (1998) Are positive interactions species-specific? Oikos 82:202–207

    Article  Google Scholar 

  • Callaway RM (2007) Positive interactions and interdependence in plant communities. Springer, Dordrecht

    Google Scholar 

  • Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848

    Article  CAS  PubMed  Google Scholar 

  • Duponnois R, Quahmane L, Kane A, Thioulouse J, Hafidi H, Boumezzough A, Prin Y, Baudoin E, Galiana A, Dreyfus B (2011) Nurse shrubs increased the early growth of Cupressus seedlings by enhancing belowground mutualism and soil microbial activity. Soil Biol Biochem 43:2160–2168

    CAS  Google Scholar 

  • Fajardo A, Mclntire EJB (2011) Under strong niche overlap conspecifics do not compete but help each other to survive: facilitation at the intraspecific level. J Ecol 99:642–650

    Google Scholar 

  • Ge GF, Li ZJ, Fan FL, Chu GX, Hou ZN, Liang YC (2010) Soil biological activity and their seasonal variations in response to long-term application of organic and inorganic fertilizers. Plant Soil 326:31–44

    Article  CAS  Google Scholar 

  • Guan SY (1986) Soil enzymes and their research methodology. Agriculture Press, Beijing, pp 274–338

    Google Scholar 

  • He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706

    Article  PubMed  Google Scholar 

  • Hortal S, Bastida F, Armas C, Lozano YM, Moreno JL, Carcía C, Pugnaire FI (2013) Soil microbial community under a nurse-plant species changes in composition, biomass and activity as the nurse grows. Soil Biol Biochem 64:139–146

    Article  CAS  Google Scholar 

  • Li JT, Duan HN, Li SP, Kuang JL, Zeng Y, Shu WS (2010) Cadmium pollution triggers a positive biodiversity-productivity relationship: evidence from a laboratory microcosm experiment. J Appl Ecol 47:890–898

    Article  CAS  Google Scholar 

  • Li SP, Li JT, Kuang JL, Duan HN, Zeng Y, Shu WS (2012) Effects of species richness on cadmium removal efficiencies of algal microcosms. J Appl Ecol 49:261–267

    Article  CAS  Google Scholar 

  • Liancourt P, Callaway RM, Michalet R (2005) Stress tolerance and competitive-response ability determine the outcome of biotic interactions. Ecology 86:1611–1618

    Article  Google Scholar 

  • Lu RK (2000) Analysis methods on soil agricultural chemistry. China Agricultural Science and Technology Press, Beijing

    Google Scholar 

  • Maestre FT, Valladares F, Reynolds JF (2006) The stress-gradient hypothesis does not fit all relationships between plant-plant interactions and abiotic stress: further insight from arid environments. J Ecol 94:17–22

    Article  Google Scholar 

  • Maestre FT, Callaway RM, Valladares F, Lortie CJ, Christopher J (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205

  • Mclntire EJB, Fajardo A (2014) Facilitation as a ubiquitous driver of biodiversity. New Phytol 201:403–416

    Article  Google Scholar 

  • Mehdawi AFE, Quinn CF, Pilon-Smits EAH (2011a) Selenium hyperaccumulators facilitate Selenium-tolerant neighbors via phytoenrichment and reduced herbivory. Curr Biol 21:1440–1449

    Article  CAS  PubMed  Google Scholar 

  • Mehdawi AFE, Quinn CF, Pilon-Smits EAH (2011b) Effects of selenium hyperaccumlation on plant-plant interactions: evidence for elemental allelopathy? New Phytol 191:120–131

    Article  CAS  PubMed  Google Scholar 

  • Mehdawi AFE, Cappa JJ, Fakra SC, Self J, Pilon-Smits EAH (2012) Interactions of selenium hyperaccumulators and nonaccumulators during cocultivation on seleniferous or nonseleniferous soil-the importance of having good neighbors. New Phytol 194:264–277

    Article  CAS  PubMed  Google Scholar 

  • Michalet R, Brooker RW, Cavieres LA, Kikvidze Z, Lortie CJ, Pugnaire FI, Valienta-Banuet A, Callaway RM (2006) Do biotic interactions shape both sides of the humped-back model of species richness in plant communities? Ecol Lett 9:767–773

    Article  PubMed  Google Scholar 

  • Michalet R, Xiao S, Touzard B, Smith DS, Cavieres LA, Callaway RM, Whitham TG (2011) Phenotypic variation in nurse traits and community feedbacks define an alpine community. Ecol Lett 14:433–443

    Article  PubMed  Google Scholar 

  • Nayar S, Miller DJ, Hunt A, Goh BPL, Chou LM (2007) Environmental effects of dredging on sediment nutrients, carbon and granulometry in a tropical estuary. Environ Monit Assess 127:1–13

    Article  CAS  PubMed  Google Scholar 

  • Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis: chemical and microbiological properties, 2nd edn. American Society of Agronomy, Inc., Wisconsin, p 1159

    Google Scholar 

  • Oviedo R, Faife-Cabrera M, Noa-Monzón A, Arroyo J, Valiente-Banuet A, Verdú M (2014) Facilitation allows plant coexistence in Cuban serpentine soils. Plant Biol 16:711–716

    Article  CAS  PubMed  Google Scholar 

  • Rey PJ, Siles G, Alcántara JM (2009) Community-level restoration profiles in Mediterranean vegetation: nurse-based vs. traditional reforestation. J Appl Ecol 46:937–945

    Article  Google Scholar 

  • Stefanowicz AM, Kapusta P, Szarek-Lukaszewska G, Grodzińska K, Niklińska M, Vogt RD (2012) Soil fertility and plant diversity enhance microbial performance in metal-polluted soils. Sci Total Environ 439:211–219

    Article  CAS  PubMed  Google Scholar 

  • Tang SR, Wilke BM, Huang CY (1999) The uptake of copper by plants dominantly growing on copper mining spoils along the Yangtze River, the People’s Republic of China. Plant Soil 209:225–232

    Article  CAS  Google Scholar 

  • van der Putten WH (2009) A multitrophic perspective on functioning and evolution of facilitation in plant communities. J Ecol 97:1131–1138

    Article  Google Scholar 

  • van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276

    Article  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DC (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Verwijmeren M, Rietkerk M, Wassen MJ, Smit C (2013) Interspecific facilitation and critical transitions in arid ecosystems. Oikos 122:341–347

    Article  Google Scholar 

  • Xiao S, Zhao L, Zhang JL, Wang XT, Chen SY (2013) The integration of facilitation into the neutral theory of community assembly. Ecol Model 251:127–134

    Article  Google Scholar 

  • Xu J, Michalet R, Zhang JL, Wang G, Chu CJ, Xiao S (2010) Assessing facilitative responses to a nurse shrub at the community level: the example of Potentilla fruticosa in a sub-alpine grassland of northwest China. Plant Biol 12:780–787

    Article  CAS  PubMed  Google Scholar 

  • Yang RY, Zan ST, Tang JJ, Chen X, Zhang Q (2010) Variation in community structure of arbuscular mycorrhizal fungi associated with a Cu tolerant plant-Elsholtzia splendens. Appl Soil Ecol 44:191–197

    Article  Google Scholar 

  • Ye ZH, Shu WS, Zhang ZQ, Lan CY, Wong MH (2002) Evaluation of major constraints to revegetation of lead/zinc mine tailings using bioassay techniques. Chemosphere 47:1103–1111

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Natural Science Foundation of China (41001368) and Anhui Provincial Natural Science Foundation (1508085SMC211). We thank Shuijin Hu, Cong Tu and two anonymous reviewers for helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. College of Environmental Science and Engineering, Anhui Normal University, South Huajin Road, Wuhu, 241003, China

    Ruyi Yang, Fuyu Guo, Shuting Zan & Gang Zhou

  2. College of Life Sciences, Zhejiang University, Hangzhou, 310058, China

    Ruyi Yang, Jianjun Tang & Xin Chen

  3. Department of Ecology, University of Marburg, Marburg, D-35043, Germany

    Wibke Wille

  4. Department of Plant and Environmental Sciences, University of Copenhagen, DK-1871, Frederiksberg, Denmark

    Jacob Weiner

Authors
  1. Ruyi Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fuyu Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shuting Zan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wibke Wille
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jianjun Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jacob Weiner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ruyi Yang.

Additional information

Responsible Editor: Henk Schat.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, R., Guo, F., Zan, S. et al. Copper tolerant Elsholtzia splendens facilitates Commelina communis on a copper mine spoil. Plant Soil 397, 201–211 (2015). https://doi.org/10.1007/s11104-015-2616-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-015-2616-0

Keywords

Search

Navigation