Skip to main content

Impacts of earthworm species on soil acidification, Al fractions, and base cation release in a subtropical soil from China

Abstract

Soil-exchangeable aluminum (Al) has toxic effects on living organisms in acidic soils. Earthworm presence and activity can alter soil pH, which has a significant influence on Al toxicity. However, the effects of earthworms on soil Al toxicity and fractions are still largely unknown. This laboratory study focused on the effects of three earthworm species (endogeics Pontoscolex corethrurus and Amynthas robustus, anecis Amynthas aspergillum) on soil acidification, Al fraction distribution, and base cation release. Three native earthworm species and a soil (latosolic red soil) collected from a botanical garden in South China were incubated under laboratory conditions. After 40 days of incubation, six Al fractions in soil, namely exchangeable (AlEx), weakly organically bound (AlOrw), organically bound (AlOr), amorphous (AlAmo), Al occluded in crystalline iron oxides (AlOxi), and amorphous aluminosilicate and gibbsite (AlAag) fractions, were extracted using a sequential procedure. Soil pH; organic carbon; total nitrogen; total Al (AlTotal); exchangeable K, Na, Ca, Mg contents; and CEC were determined as well. Compared to control soil, pH values increased by 0.79, 0.41, and 0.57 units in casts in the presence of P. corethrurus, A. robustus, and A. aspergillum, and 0.70, 0.32, and 0.50 units in non-ingested soil, respectively. Compared to control soil, the 61.7%, 30.7%, and 36.1% of AlEx contents in casts and 68.5%, 25.9%, and 39.0% of AlEx in non-ingested soil significantly decreased with the addition of P. corethrurus, A. robustus, and A. aspergillum, respectively. Moreover, compared to control soil, the 78.7%, 37.7%, and 40.1% of exchangeable Ca2+ and 12.3%, 24.7%, and 26.8% of exchangeable Mg2+ contents in casts significantly increased with the presence of P. corethrurus, A. robustus, and A. aspergillum, respectively. Soil treated with P. corethrurus had higher soil pH values, exchangeable Ca2+ contents, and lower AlEx than those with A. robustus and A. aspergillum. Results of principal component analyses showed that P. corethrurus, A. robustus, and A. aspergillum casts and non-ingested soil differ for soil pH, Al fractions, and exchangeable base cations release. These results indicate that earthworms, especially P. corethrurus, can reduce soil Al toxicity, increase soil pH, and affect the release of exchangeable base cations.

This is a preview of subscription content, access via your institution.

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

References

  1. Álvarez E, Fernández-Sanjurjo MJ, Núñez A, Seco N, Corti G (2012) Aluminium fractionation and speciation in bulk and rhizosphere of a grass soil amended with mussel shells or lime. Geoderma 173-174:322–329

    Google Scholar 

  2. Bailey SW, Horsley SB, Long RP (2005) Thirty years of change in forest soils of the Allegheny plateau, Pennsylvania. Soil Sci Soc Am J 69:681–690

    CAS  Google Scholar 

  3. Baquy AA, Li JY, Jiang J, Mehmood K, Shi RY, Xu RK (2018) Critical pH and exchangeable Al of four acidic soils derived from different parent materials for maize crops. J Soils Sediments 18:1490–1499

    CAS  Google Scholar 

  4. Basker A, Kirkman JH, Macgregor AN (1994) Changes in potassium availability and other soil properties due to soil ingestion by earthworms. Biol Fertil Soils 17:154–157

    CAS  Google Scholar 

  5. Benckiser G (1997) Fauna in soil ecosystems recycling processes, nutrient fluxes, and agricultural production. Marcel Dekker. Madison, New York, pp 173–225

    Google Scholar 

  6. Blouin M, Hodson ME, Delgado EA, Baker G, Brussaard L, Butt KR, Dai J, Dendooven L, Peres G, Tondoh JE, Cluzeau D, Brun JJ (2013) A review of earthworm impact on soil function and ecosystem services. Eur J Soil Sci 64:161–182

    Google Scholar 

  7. Bossuyt H, Six J, Hendrix PF (2005) Protection of soil carbon by microaggregates within earthworm casts. Soil Biol Biochem 37:251–258

    CAS  Google Scholar 

  8. Briones MJI, Ostle NJ, Piearce TG (2008) Stable isotopes reveal that the calciferous gland of earthworms is a CO2-fixing organ. Soil Biol Biochem 40:554–557

    CAS  Google Scholar 

  9. Chan KY, Mead JA (2003) Soil acidity limits colonisation by Aporrectodea trapezoides, an exotic earthworm. Pedobiologia 47:225–229

    Google Scholar 

  10. Cortet J, Vauflery AGD, Balaguer NP, Gomot L, Texier C, Cluzeau D (1999) The use of invertebrate soil fauna in monitoring pollutant effects. Eur J Soil Biol 35:115–134

    CAS  Google Scholar 

  11. Dai J, Becquer T, Rouiller JH, Reversat G, Bernhard-Reversat F, Nahmani J, Lavelle P (2004) Heavy metal accumulation by two earthworm species and its relationship to total and DTPA-extractable metals in soils. Soil Biol Biochem 36:91–98

    CAS  Google Scholar 

  12. Evans AJR, Jacobs MB (2016) Aluminum activity in alpine tundra soil, Rocky Mountain National Park, Colorado, U.S.A. Soil Sci 181:359–367

    CAS  Google Scholar 

  13. García-Montero LG, Valverde-Asenjo I, Grande-Ortíz MA, Menta C, Hernando I (2013) Impact of earthworm casts on soil pH and calcium carbonate in black truffle burns. Agrofor Syst 87:815–826

    Google Scholar 

  14. Gestel VCAM, Hoogerwerf G (2001) Influence of soil pH on the toxicity of aluminium for Eisenia andrei (Oligochaeta: Lumbricidae) in an artificial soil substrate. Pedobiologia 45:385–395

    Google Scholar 

  15. Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010

    CAS  Google Scholar 

  16. Hagvall K, Persson P, Karlsson T (2015) Speciation of aluminum in soils and stream waters: the importance of organic matter. Chem Geol 417:32–43

    CAS  Google Scholar 

  17. Hodson ME, Donner E (2013) Managing adverse soil chemical environments. In: Gregory PJ, Nortcliff S (eds) Soil conditions and plant growth. Blackwell, Chichester, pp 195–237

    Google Scholar 

  18. Huang JH, Zhang WX, Liu MY, Briones MJI, Eisenhauer N, Shao YH, Cai XA, Fu SL, Xia HP (2015) Different impacts of native and exotic earthworms on rhizodeposit carbon sequestration in a subtropical soil. Soil Biol Biochem 90:152–160

    CAS  Google Scholar 

  19. Jou ASR, Kamprath EJ (1979) Copper chloride as an extractant for estimating the potentially reactive aluminum pool in acid soils. Soil Sci Soc Am J 43:35–38

    Google Scholar 

  20. Karaca A (2011) Biology of earthworms. Chapman & Hall, London, pp 51–67

    Google Scholar 

  21. Kubová J, Matúš P, Bujdoš M, Medved J (2005) Influence of acid mining activity on release of aluminum to the environment. Anal Chim Acta 547:119–125

    Google Scholar 

  22. Kunito T, Isomura I, Sumi H, Park HD, Toda H, Otsuka S, Nagaoka K, Saeki K, Senoo K (2016) Aluminum and acidity suppress microbial activity and biomass in acidic forest soils. Soil Biol Biochem 97:23–30

    CAS  Google Scholar 

  23. Larssen T, Vogt RD, Seip HM, Furuberg G, Liao JS, Xiong JL (1999) Mechanisms for aluminum release in Chinese acid forest soils. Geoderma 91:65–86

    CAS  Google Scholar 

  24. Lavelle P, Spain AV (2001) Soil ecology. Kluwer Scientific Publications, Dordrecht, pp 288–298

    Google Scholar 

  25. Li JY, Xu RK, Tiwari D, Ji GL (2006) Mechanism of aluminum release from variable charge soils induced by low-molecular-weight organic acids: kinetic study. Geoderma 70:2755–2764

    CAS  Google Scholar 

  26. Lin Z, Li XM, Li YT, Huang DY, Dong J, Li FB (2012) Enhancement effect of two ecological earthworm species (Eisenia foetida and Amynthas robustus E. Perrier) on removal and degradation processes of soil DDT. J Environ Monit 14:1551–1558

    CAS  Google Scholar 

  27. Moro H, Kunito T, Saito T, Yaguchi N, Sato T (2014) Soil microorganisms are less susceptible than crop plants to potassium deficiency. Arch Agron Soil Sci 60:1807–1813

    CAS  Google Scholar 

  28. Müller F (1857) Lumbricus corethrurus. Burstenschwanz. Archiv Fur Naturg 23: 6–113

    Google Scholar 

  29. Perrier E (1872) Lombriciens Terrestres. Nouvelles Archives Du Museum. 4-192

  30. Pierart A, Dumat C, Maes AQ, Roux C, Sejalon-Delmas N (2018) Opportunities and risks of biofertilization for leek production in urban areas: influence on both fungal diversity and human bioaccessibility of inorganic pollutants. Sci Total Environ 624:1140–1151

    CAS  Google Scholar 

  31. Qiao X, Xiao WY, Jaffe D, Kota SH, Ying Q, Tang Y (2015) Atmospheric wet deposition of sulfur and nitrogen in Jiuzhaigou National Nature Reserve, Sichuan Province, China. Sci Total Environ 511:28–36

    CAS  Google Scholar 

  32. R Development Core Team (2007) R: a language and environment for statistical computing, Vienna, Austria. (ISBN 3–900051–07-0). http://www.R-project.org

  33. Richardson JB, Blossey B, Dobson AM (2018) Earthworm impacts on trace metal (Al, Fe, Mo, Cu, Zn, Pb) exchangeability and uptake by young Acer saccharum and Polystichum acrostichoides. Biogeochemistry 138:103–119

    CAS  Google Scholar 

  34. Salmon S (2001) Earthworm excreta (mucus and urine) affect the distribution of springtails in forest soils. Biol Fertil Soils 34:304–310

    CAS  Google Scholar 

  35. Shao ZC, He Q, Wang WJ (1998) Forms of aluminum in red soils. Acta Pedol Sin 35:38–48 (in Chinese with English abstract)

    CAS  Google Scholar 

  36. Shao YH, Zhang WX, Eisenhauer N, Liu T, Xiong YM, Liang CF, Fu SL (2017) Nitrogen deposition cancels out exotic earthworm effects on plant-feeding nematode communities. J Anim Ecol 86:708–717

    Google Scholar 

  37. Sizmur T, Hodson ME (2009) Do earthworms impact metal mobility and availability in soil? - a review. Environ Pollut 157:1981–1989

    CAS  Google Scholar 

  38. Sizmur T, Palumbo-Roe B, Hodson ME (2011) Impact of earthworms on trace element solubility in contaminated mine soils amended with green waste compost. Environ Pollut 159:1852–1860

    CAS  Google Scholar 

  39. SSIR (2004) Soil survey laboratory methods manual, soil survey investigations report, version 4.0 ed. United States Department of Agriculture, USA, pp 173–177

    Google Scholar 

  40. Ščančar J, Milačič R (2006) Aluminium speciation in environmental samples: a review. Anal Bioanal Chem 386:999–1012

    Google Scholar 

  41. Thioulouse J, Chessel D, Dolédec S, Olivier JM (1997) ADE-4: a multivariate analysis and graphical display software. Stat Comput 7:75–83

    Google Scholar 

  42. Tica D, Udovic M, Lestan D (2013) Long-term efficiency of soil stabilization with apatite and Slovakite: the impact of two earthworm species (Lumbricus terrestris and Dendrobaena veneta) on lead bioaccessibility and soil functioning. Chemosphere 91:1–6

    CAS  Google Scholar 

  43. Udovic M, Lestan D (2007) The effect of earthworms on the fractionation and bioavailability of heavy metals before and after soil remediation. Environ Pollut 148:663–668

    CAS  Google Scholar 

  44. Wang AQ, Lin K, Ma CX, Gao Q, Zhu QF, Ji XJ, Zhang G, Xue L, Zu CL, Jiang CQ, Shen J, Li DC (2018) A brief study on pH, exchangeable Ca2+ and Mg2+ in farmlands under tobacco-rice rotation in Xuancheng city of South Anhui. Agric Sci 9:480–488

    CAS  Google Scholar 

  45. Wen B, Liu Y, Hu XY, Shan XQ (2006) Effect of earthworms (Eisenia fetida) on the fractionation and bioavailability of rare earth elements in nine Chinese soils. Chemosphere 63:1179–1186

    CAS  Google Scholar 

  46. Xu RK (2012) Amelioration principles and technologies for acidified red soils. Science Press, Beijing, pp 1–6

    Google Scholar 

  47. Yu XZ, Cheng JM, Wong MH (2005) Earthworm-mycorrhiza interaction on Cd uptake and growth of ryegrass. Soil Biol Biochem 37:195–201

    CAS  Google Scholar 

  48. Zhang BG, Li GT, Shen TS, Wang JK, Sun Z (2000) Changes in microbial biomass C, N, and P and enzyme activities in soil incubated with the earthworms Metaphire guillelmi or Eisenia fetida. Soil Biol Biochem 32:2055–2062

    CAS  Google Scholar 

  49. Zhang C, Langlest R, Velasquez E, Pando A, Brunet D, Dai J, Lavelle P (2009) Cast production and NIR spectral signatures of Aporrectodea caliginosa fed soil with different amounts of half-decomposed Populus nigra litter. Biol Fertil Soils 45:839–844

    Google Scholar 

  50. Zhang JE, Yu JY, Ouyang Y, Xu HQ (2013) Responses of earthworm to aluminum toxicity in latosol. Environ Sci Pollut Res 20:1135–1141

    Google Scholar 

  51. Zhang C, Mora P, Dai J, Chen XF, Giusti-Miller S, Ruiz-Camacho N, Velasquez E, Lavelle P (2016) Earthworm and organic amendment effects on microbial activities and metal availability in a contaminated soil from China. Appl Soil Ecol 104:54–66

    Google Scholar 

  52. Zhao Y, Duan L, Xing J, Larssen T, Nielsen PC, Hao JM (2009) Soil acidification in China: is controlling SO2 emissions enough? Environ Sci Technol 43:8021–8026

    CAS  Google Scholar 

Download references

Acknowledgements

Thanks to Qijun Yang, Haoyu Wang, and Huan Qian for laboratory assistance.

Funding

This research was supported by the Natural Science Foundation of China (Grant No. 41201305 and 41601227) and National Key Research and Development Program of China (2016YFD0201301 and 2016YFD0201200).

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Chi Zhang or Jun Dai.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Highlights

P. corethrurus decreased 61.7% exchangeable Al content significantly in cast compared to control soil.

P. corethrurus was more effective to reduce soil acidification than A. robustus and A. aspergillum.

• Casts had higher exchangeable Ca2+, Mg2+, K+, CEC, TN, and SOC than non-ingested soil for the three earthworms.

Responsible editor: Zhihong Xu

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wu, J., Zhang, C., Xiao, L. et al. Impacts of earthworm species on soil acidification, Al fractions, and base cation release in a subtropical soil from China. Environ Sci Pollut Res 27, 33446–33457 (2020). https://doi.org/10.1007/s11356-019-05055-8

Download citation

Keywords

  • Earthworms
  • Aluminum fractions
  • Soil pH
  • Exchangeable base cations
  • Latosolic red soil