Ecological Research

, Volume 32, Issue 4, pp 603–610 | Cite as

Does an earthworm species acclimatize and/or adapt to soil calcium conditions? The consequences of soil nitrogen mineralization in forest soil

Original Article

Abstract

Calcium (Ca)-rich food can increase feeding of Lumbricidae. Earthworms can be genetically differentiated at a small spatial scale and acclimatize to the local environment during growth. Soil feeding and subsequent cast production by earthworms affects soil N mineralization. Here, we hypothesized that soil feeding and subsequent cast production by Lumbricidae species increases with high soil Ca content and that this increase is stronger in worms from high-Ca soil. We also hypothesized that changes in the soil feeding of Lumbricidae species along with the Ca content affects the soil N mineralization via changes in the cast production. Using a geophageous earthworm species (Eisenia japonica) originated from two different Ca environments (calcareous soil and sedimentary soil), we investigated cast production and soil N mineralization in three soils (sedimentary soil, sedimentary soil with Ca addition, and calcareous soil). The soil feeding of E. japonica from both origins did not always increase despite the high soil Ca content. We suggest that both the Ca content and other soil conditions (e.g., soil C:N) might be major factors in increasing soil feeding by E. japonica. Furthermore, the influence of Ca addition on cast production varied according to the earthworm origin. As expected, these differences in cast production are linked to soil N mineralization (especially nitrification). In summary, our study suggests that the acclimatization and/or adaptation of Lumbricidae species to local environmental factors not only soil Ca content explains spatially heterogeneous soil N mineralization in forest soil.

Keywords

Biogeochemistry Stoichiometry Nitrogen dynamics Evolution Aggregate 

Notes

Acknowledgements

We acknowledge Mr. T. Miura in Nakatonbetsu Town and the technical staff of Tesio Experimental Forest of Hokkaido University for their support during the research. We also sincerely thank Dr. K. Takagi, Professor Y. Hashidoko, Ms. R. Isoda and Ms. E. Marumo for their comments on this project. The analysis of soil and earthworm samples was carried out with ICPE-9000 at the OPEN FACILITY, Hokkaido University Sousei Hall. This project is financially supported by JSPS for young researchers (Type B to K.M.) and by the Kuribayashi Ikuei Foundation.

Supplementary material

11284_2017_1473_MOESM1_ESM.pdf (79 kb)
Supplementary material 1 (PDF 79 kb)

References

  1. Auclerc A, Nahmani J, Huguier P, Capowiez Y, Aran D, Guérold F (2011) Adapting ecotoxicological tests based on earthworm behavior to assess the potential effectiveness of forest soil liming. Pedobiologia (Jena) 54:63–68CrossRefGoogle Scholar
  2. Berg M, De Ruiter P, Didden W, Janssen M, Schouten T, Verhoef H (2001) Community food web, decomposition and nitrogen mineralisation in a stratified Scots pine forest soil. Oikos 94:130–142CrossRefGoogle Scholar
  3. Blanchart E (1992) Restoration by earthworms (megascolecidae) of the macroaggregate structure of a destructured savanna soil under field conditions. Soil Biol Biochem 24:1587–1594CrossRefGoogle Scholar
  4. David JF, Gillon D (2009) Combined effects of elevated temperatures and reduced leaf litter quality on the life-history parameters of a saprophagous macroarthropod. Glob Chang Biol 15:156–165CrossRefGoogle Scholar
  5. Dupont L, Gresille Y, Richard B, Decaëns T, Mathieu J (2015) Dispersal constraints and fine-scale spatial genetic structure in two earthworm species. Biol J Linn Soc 114:335–347CrossRefGoogle Scholar
  6. Edwards CA (2004) Earthworm ecology, 2nd edn. CRC, FloridaCrossRefGoogle Scholar
  7. Edwards CA, Bohlen PJ (1996) Biology and ecology of earthworms, 3rd edn. Chapman and Hall, LondonGoogle Scholar
  8. Hillebrand H, Borer ET, Bracken MES, Cardinale BJ, Cebrian J, Cleland EE, Elser JJ, Gruner DS, Stanley Harpole W, Ngai JT, Sandin S, Seabloom EW, Shurin JB, Smith JE, Smith MD (2009) Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems. Ecol Lett 12:516–527CrossRefPubMedGoogle Scholar
  9. Holdsworth AR, Frelich LE, Reich PB (2012) Leaf litter disappearance in earthworm-invaded Northern Hardwood forests: role of tree species and the chemistry and diversity of litter. Ecosystems 15:913–926CrossRefGoogle Scholar
  10. Ishizuka K (2014) Pictorial book of earthworm. National Rural Education Association, TokyoGoogle Scholar
  11. Kawaguchi T, Kyoshima T, Kaneko N (2011) Mineral nitrogen dynamics in the casts of epigeic earthworms (Metaphire hilgendorfi: Megascolecidae). Soil Sci Plant Nutr 57:387–395CrossRefGoogle Scholar
  12. Kharin SA, Kurakov AV (2009) Transformation of nitrogen compounds and dynamics of microbial biomass in fresh casts of Aporrectodea caliginosa. Eurasian Soil Sci 42:75–81CrossRefGoogle Scholar
  13. Lavelle P, Bignell D, Lepage M, Wolters W, Roger P, Ineson P, Heal OW, Dhillion S (1997) Soil function in a changing world: the role of invertebrate ecosystem engineers. Eur J Soil Biol 33:159–193Google Scholar
  14. Makoto K, Minamiya Y, Kaneko N (2016) Differences in soil type drive the intraspecific variation in the responses of an earthworm species and consequently, tree growth to warming. Plant Soil 404:209–218CrossRefGoogle Scholar
  15. Marhan S, Auber J, Poll C (2015) Additive effects of earthworms, nitrogen-rich litter and elevated soil temperature on N2O emission and nitrate leaching from an arable soil. Appl Soil Ecol 86:55–61CrossRefGoogle Scholar
  16. Milcu A, Manning P (2011) All size classes of soil fauna and litter quality control the acceleration of litter decay in its home environment. Oikos 120:1366–1370CrossRefGoogle Scholar
  17. Nakamura Y (1972) Ecological studies on the Family Lumbricidae from Hokkaido I, ecological distribution. Jpn Soc Appl Entomol Zool 16:18–23CrossRefGoogle Scholar
  18. Ott D, Rall BC, Brose U (2012) Climate change effects on macrofaunal litter decomposition: the interplay of temperature, body masses and stoichiometry. Philos Trans R Soc B Biol Sci 367:3025–3032CrossRefGoogle Scholar
  19. Scheu S (1987) The influence of earthworms (Lumbricidae) on the nitrogen dynamics in the soil litter system of a deciduous forest. Oecologia 72:197–201CrossRefPubMedGoogle Scholar
  20. Simon A, Sivasithamparam K (1989) Pathogen-suppression—a case-study in biological suppression of gaeumannomyces-graminis var tritici in soil. Soil Biol Biochem 21:331–337CrossRefGoogle Scholar
  21. Springett JA, Syers JK (1984) Effect of pH and calcium content of soil on earthworm cast production in the laboratory. Soil Biol Biochem 16:185–189CrossRefGoogle Scholar
  22. Sullivan TJ, Dreyer AP, Peterson JW (2009) Genetic variation in a subterranean arthropod (Folsomia candida) as a method to identify low-permeability barriers in an aquifer. Pedobiologia (Jena) 53:99–105CrossRefGoogle Scholar
  23. Toyota A, Hynšt J, Cajthaml T, Frouz J (2013) Soil fauna increase nitrogen loss in tilled soil with legume but reduce nitrogen loss in non-tilled soil without legume. Soil Biol Biochem 60:105–112CrossRefGoogle Scholar
  24. Vitousek PM, Hättenschwiler S, Olander L, Allison S (2002) Nitrogen and nature. Ambio 31:97–101CrossRefPubMedGoogle Scholar

Copyright information

© The Ecological Society of Japan 2017

Authors and Affiliations

  1. 1.Graduate School of Environmental ScienceHokkaido UniversityHoronobeJapan
  2. 2.Teshio Experimental Forest, Field Science Center for Northern BiosphereHokkaido UniversityHoronobeJapan

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