Advertisement

Biology and Fertility of Soils

, Volume 55, Issue 3, pp 213–227 | Cite as

Exotic earthworms maintain soil biodiversity by altering bottom-up effects of plants on the composition of soil microbial groups and nematode communities

  • Yuanhu Shao
  • Weixin Zhang
  • Nico Eisenhauer
  • Tao Liu
  • Olga Ferlian
  • Xiaoli Wang
  • Yanmei Xiong
  • Chenfei Liang
  • Shenglei FuEmail author
Original Paper
  • 285 Downloads

Abstract

Bottom-up effects of plants on soil communities can be modified by the activity of exotic earthworms, by altering resource availability for soil food webs through feeding, burrowing, and casting activities. The present study explored effects of plants (planting of shrubs) on soil micro-food webs (composition of soil microbial and nematode communities), and whether these effects were altered by the activity of exotic earthworms (exotic earthworms addition). Planted shrubs resulted in a non-significant increase of bacterial biomass and significantly increased the abundance of different nematode trophic groups and total nematode biomass, indicating that planted shrubs had significant bottom-up effects on soil bacteria and nematodes. Planted shrubs decreased nematode diversity, evenness, and richness, but increased nematode dominance in the plots where the abundance of exotic earthworms was not amended. By contrast, these effects of shrub presence on soil biodiversity were not found in the plots that received exotic earthworms. In addition, planted shrubs increased the total energy flux to the nematode community. By contrast, the elevated activity of exotic earthworms mitigated the increase in total energy flux to nematodes in the presence of shrubs, and increased the ratio of fungal to bacterial PLFAs. Both of these changes indicate reduced energy flux in the plots with added exotic earthworms. Nematode diversity decreased, while nematode dominance increased with increasing total energy flux to nematodes, probably because few species benefited from high energy flux. Our study indicates that exotic earthworms can maintain soil biodiversity by reducing the energy flux through soil food webs.

Keywords

Soil nematodes Soil micro-food webs Exotic earthworms Bottom-up effects Energy flux Microbial PLFAs 

Notes

Acknowledgments

We are grateful to Yongxing Li for his help during soil sampling. The authors are grateful to Prof. Wenju Liang, Prof. Paolo Nannipieri, and two anonymous reviewers for the helpful comments.

Funding information

This study was funded by the Natural Science Foundation of China (31470559), Zhongyuan Scholar Program (182101510005), and “Heshan National Field Research Station of Forest Ecosystem”. NE and OF acknowledge support from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement no 677232 to NE). Further support came from the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, funded by the German Research Foundation (FZT 118).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

374_2019_1343_MOESM1_ESM.docx (124 kb)
ESM 1 (DOCX 123 kb)
374_2019_1343_MOESM2_ESM.xlsx (22 kb)
ESM 2 (XLSX 22 kb)

References

  1. Aho K, Derryberry D, Peterson T (2014) Model selection for ecologists: the worldviews of AIC and BIC. Ecology 95:631–636CrossRefGoogle Scholar
  2. Barker KR (1985) Nematode extraction and bioassays. In Barker KR, Carter CC, Sasser JN (Eds). An advanced treatise on meloidogyne, Volume 2. Methodology. North Carolina State University Graphics, Raleigh, NC, pp 19–35Google Scholar
  3. Barnes AD, Jochum M, Mumme S, Haneda NF, Farajallah A, Widarto TH, Brose U (2014) Consequences of tropical land use for multitrophic biodiversity and ecosystem functioning. Nat Commun 5:5351CrossRefGoogle Scholar
  4. Bongers T, Bongers M (1998) Functional diversity of nematodes. Appl Soil Ecol 10:239–251CrossRefGoogle Scholar
  5. Bongers T, Ferris H (1999) Nematode community structure as a bioindicator in environmental monitoring. Trends Ecol Evol 14:224–228CrossRefGoogle Scholar
  6. Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278CrossRefGoogle Scholar
  7. Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12CrossRefGoogle Scholar
  8. Brown GG (1995) How do earthworms affect microfloral and faunal community diversity? Plant Soil 170:209–231CrossRefGoogle Scholar
  9. Caporaso JG, Lauber CL, Walters WA, Berglyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16s rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A 108:4516–4522CrossRefGoogle Scholar
  10. Čoja T, Zehetner K, Bruckner A, Watzinger A, Meyer E (2008) Efficacy and side effects of five sampling methods for soil earthworms (Annelida, Lumbricidae). Ecotoxicol Environ Saf 71:552–565CrossRefGoogle Scholar
  11. Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of soil ecology (2nd ed.). Academic Press, San DiegoGoogle Scholar
  12. De Beeck MO, Lievens B, Busschaert P, Declerck S, Vangronsveld J, Colpaert JV (2014) Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PLoS One 9:e97629CrossRefGoogle Scholar
  13. De Long JR, Dorrepaal E, Kardol P, Nilsson MC, Teuber LM, Wardle DA (2016) Contrasting responses of soil microbial and nematode communities to warming and plant functional group removal across a post-fire boreal forest successional gradient. Ecosystems 19:339–355CrossRefGoogle Scholar
  14. De Ruiter PC, Neutel AM, Moore JC (1995) Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269:1257–1260CrossRefGoogle Scholar
  15. Dennis PG, Miller AJ, Hirsch PR (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72:313–327CrossRefGoogle Scholar
  16. Ehnes RB, Rall BC, Brose U (2011) Phylogenetic grouping, curvature and metabolic scaling in terrestrial invertebrates. Ecol Lett 14:993–1000CrossRefGoogle Scholar
  17. Eisenhauer N (2010) The action of an animal ecosystem engineer: identification of the main mechanisms of earthworm impacts on soil microarthropods. Pedobiologia 53:343–352CrossRefGoogle Scholar
  18. Eisenhauer N, Partsch S, Parkinson D, Scheu S (2007) Invasion of a deciduous forest by earthworms: changes in soil chemistry, microflora, microarthropods and vegetation. Soil Biol Biochem 39:1099–1110CrossRefGoogle Scholar
  19. Eisenhauer N, Milcu A, Sabais ACW, Scheu S (2008) Animal ecosystem engineers modulate the diversity-invasibility relationship. PLoS One 3:e3489CrossRefGoogle Scholar
  20. Eisenhauer N, Milcu A, Nitschke N, Sabais ACW, Scherber C, Scheu S (2009) Earthworm and belowground competition effects on plant productivity in a plant diversity gradient. Oecologia 161:291–301CrossRefGoogle Scholar
  21. FAO (2006) World reference base for soil resources 2006 (2nd ed.). World Soil Resources Reports NO.103. FAO, RomeGoogle Scholar
  22. Ferlian O, Eisenhauer N, Aguirrebengoa M, Camara M, Ramirez-Rojas I, Santos F, Tanalgo K, Thakur M (2018) Invasive earthworms erode soil biodiversity: a meta-analysis. J Anim Ecol 87:162–172CrossRefGoogle Scholar
  23. Ferris H, Bongers T (2006) Nematode indicators of organic enrichment. J Nematol 38:3–12Google Scholar
  24. Ferris H, Tuomisto H (2015) Unearthing the role of biological diversity in soil health. Soil Biol Biochem 85:101–109CrossRefGoogle Scholar
  25. Freckman DW (1988) Bacterivorous nematodes and organic-matter decomposition. Agric Ecosyst Environ 24:195–217CrossRefGoogle Scholar
  26. Fu SL, Ferris H, Brown D, Plant R (2005) Does the positive feedback effect of nematodes on the biomass and activity of their bacteria prey vary with nematode species and population size? Soil Biol Biochem 37:1979–1987CrossRefGoogle Scholar
  27. Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378CrossRefGoogle Scholar
  28. Hendrix PF, Callaham JMA, Drake J, Huang CY, James SW, Snyder BA, Zhang W (2008) Pandora’s box contained bait: the global problem of introduced earthworms. Annu Rev Ecol Evol Syst 39:593–613CrossRefGoogle Scholar
  29. Holtkamp R, Kardol P, van der Wal A, Dekker SC, van der Putten WH, de Ruiter PC (2008) Soil food web structure during ecosystem development after land abandonment. Appl Soil Ecol 39:23–34CrossRefGoogle Scholar
  30. 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 90:152–160CrossRefGoogle Scholar
  31. Hugot JP, Baujard P, Morand S (2001) Biodiversity in helminths and nematodes as a field of study: an overview. Nematology 3:199–208CrossRefGoogle Scholar
  32. Kozdrój J, van Elsas JD (2000) Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biol Biochem 32:1405–1417CrossRefGoogle Scholar
  33. Lapied E, Lavelle P (2003) The peregrine earthworm Pontoscolex corethrurus in the East coast of Costa Rica. Pedobiologia 47:471–474Google Scholar
  34. Lavelle P, Melendez G, Pashanasi B, Schaefer R (1992) Nitrogen mineralization and reorganization in casts of the geophagous tropical earthworm Pontoscolex corethrurus (glossoscolecidae). Biol Fertil Soils 14:49–53CrossRefGoogle Scholar
  35. Lavelle P, Decaëns T, Aubert M, Barot S, Blouin M, Bureau F, Margerie P, Mora P, Rossi JP (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:S3–S15CrossRefGoogle Scholar
  36. Liu Z, Zou X (2002) Exotic earthworms accelerate plant litter decomposition in a Puerto Rican pasture and a wet forest. Ecol Appl 12:1406–1417CrossRefGoogle Scholar
  37. Lv M, Shao Y, Lin Y, Liang C, Dai J, Liu Y, Fan P, Zhang W, Fu S (2016) Plants modify the effects of earthworms on the soil microbial community and its activity in a subtropical ecosystem. Soil Biol Biochem 103:446–451CrossRefGoogle Scholar
  38. Moore JC (1994) Impact of agriculture practices on soil food web structure: theory and application. Agric Ecosyst Environ 51:239–247CrossRefGoogle Scholar
  39. Moore JC, de Ruiter PC, Hunt HW, Coleman DC, Freckman DW (1996) Microcosms and soil ecology: critical linkages between fields studies and modelling food webs. Ecology 77:694–705CrossRefGoogle Scholar
  40. Nechitaylo TY, Yakimov MM, Godinho M, Timmis KN, Belogolova E, Byzov BA, Kurakov AV, Jones DL, Golyshin PN (2010) Effect of the earthworms Lumbricus terrestris and Aporrectodea caliginosa on bacterial diversity in soil. Microb Ecol 59:574–587CrossRefGoogle Scholar
  41. Neher DA (2010) Ecology of plant and free-living nematodes in natural and agricultural soil. Annu Rev Phytopathol 48:371–394CrossRefGoogle Scholar
  42. Neher DA, Darby BJ (2006) Computation and application of nematode community indices: general guidelines. In: Eyualem A, Traunspurger W, Andrassy I (eds) Freshwater Nematodes: Ecology and Taxonomy. CAB International, Wallingford, pp 211–222CrossRefGoogle Scholar
  43. Paterson E, Osler G, Dawson LA, Gebbing T, Sim A, Ord B (2008) Labile and recalcitrant plant fractions are utilised by distinct microbial communities in soil: independent of the presence of roots and mycorrhizal fungi. Soil Biol Biochem 40:1103–1113CrossRefGoogle Scholar
  44. Pollierer MM, Langel R, Körner C, Maraun M, Scheu S (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736CrossRefGoogle Scholar
  45. R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  46. Rhea-Fournier (2012) The relationship of earthworms and soil carbon, nitrogen, and microbial biomass in a subtropical wet forest in Puerto Rico. MS thesis. University of Puerto Rico – Río PiedrasGoogle Scholar
  47. Rooney N, McCann KS (2012) Integrating food web diversity, structure and stability. Trends Ecol Evol 27:40–46CrossRefGoogle Scholar
  48. Rooney N, McCann K, Gellner G, Moore JC (2006) Structural asymmetry and the stability of diverse food webs. Nature 442:265–269CrossRefGoogle Scholar
  49. Scheu S (2003) Effect of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:846–856Google Scholar
  50. Scheu S, Ruess L, Bonkowski M (2005) Interactions between micro-organisms and soil micro- and mesofauna. In: Buscot F, Varma A (eds) Microorganisms in soils: roles in genesis and function. Springer-Verlag, Berlin, pp 253–275CrossRefGoogle Scholar
  51. Scheunemann N, Maraun M, Scheu S, Butenschoen O (2015) The role of shoot residues vs. crop species for soil arthropod diversity and abundance of arable systems. Soil Biol Biochem 81:81–88CrossRefGoogle Scholar
  52. Schöler A, Jacquiod S, Vestergaard G, Schulz S, Schloter M (2017) Analysis of soil microbial communities based on amplicon sequencing of marker genes. Biol Fertil Soils 53:485–489CrossRefGoogle Scholar
  53. Schwarz B, Barnes AD, Thakur MP, Brose U, Ciobanu M, Reich PB, Rich RL, Rosenbaum B, Stefanski A, Eisenhauer N (2017) Warming alters energetic structure and function but not resilience of soil food webs. Nat Clim Chang 7:895–900CrossRefGoogle Scholar
  54. Schwarzmüller F, Eisenhauer N, Brose U (2015) ‘Trophic whales’ as biotic buffers: weak interactions stabilize ecosystems against nutrient enrichment. J Anim Ecol 84:680–691CrossRefGoogle Scholar
  55. Shao Y, Wang X, Zhao J, Wu J, Zhang W, Neher DA, Li Y, Lou Y, Fu S (2016) Subordinate plants sustain the complexity and stability of soil micro-food webs in natural bamboo forest ecosystems. J Appl Ecol 53:130–139CrossRefGoogle Scholar
  56. Shao Y, Zhang W, Eisenhauer N, Liu T, Xiong Y, Liang C, Fu S (2017) Nitrogen deposition cancels out exotic earthworm effects on plant-feeding nematode communities. J Anim Ecol 86:708–717CrossRefGoogle Scholar
  57. Shao Y, Liu T, Eisenhauer N, Zhang W, Wang X, Xiong Y, Liang C, Fu S (2018) Plants mitigate detrimental nitrogen deposition effects on soil biodiversity. Soil Biol Biochem 127:178–186CrossRefGoogle Scholar
  58. Szlavecz K, Pitz SL, Bernard MJ, Xia LJ, O’Neill JP, Chang CH, McCormick MK, Whigham DF (2013) Manipulating earthworm abundance using electroshocking in deciduous forests. Pedobiologia 56:33–40CrossRefGoogle Scholar
  59. Van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefGoogle Scholar
  60. Vestergaard G, Schulz S, Schöler A, Schloter M (2017) Making big data smart—how to use metagenomics to understand soil quality. Biol Fertil Soils 53:479–484CrossRefGoogle Scholar
  61. Wardle DA (2002) Communities and ecosystems—linking the aboveground and belowground components. Princeton University PressGoogle Scholar
  62. Wardle DA (2005) How plant communities influence decomposer communities. In: Bardgett RD, Usher MB, Hopkins DW (eds) Biological diversity and function in soils. Cambridge University Press, Cambridge, pp 119–138CrossRefGoogle Scholar
  63. Wardle DA (2006) The influence of biotic interactions on soil biodiversity. Ecol Lett 9:870–886CrossRefGoogle Scholar
  64. Wardle DA, Bardgett RD, Callaway RM, Van der Putten WH (2011) Terrestrial ecosystem responses to species gains and losses. Science 332:1273–1277CrossRefGoogle Scholar
  65. Yeates GW (1979) Soil nematodes in terrestrial ecosystems. J Nematol 11:213–229Google Scholar
  66. Yeates GW (1999) Effects of plants on nematode community structure. Annu Rev Phytopathol 37:127–149CrossRefGoogle Scholar
  67. Yeates GW (2007) Abundance, diversity, and resilience of nematode assemblages in forest. Can J For Res 37:216–225CrossRefGoogle Scholar
  68. Yeates GW, Bongers T (1999) Nematode diversity in agroecosystems. Agric Ecosyst Environ 74:113–135CrossRefGoogle Scholar
  69. Yeates GW, Bongers T, De Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera—an outline for soil ecologists. J Nematol 25:315–331Google Scholar
  70. Zaller JG, Arnone JA (1997) Activity of surface-casting earthworms in a calcareous grassland under elevated atmospheric CO2. Oecologia 111:249–254CrossRefGoogle Scholar
  71. Zhang W, Li J, Guo M, Liao C (2005) Seasonal variation of the earthworm community structure as correlated with environmental factors in three plantations of Heshan, Guangdong, China. Acta Ecol Sin 25:1362–1370Google Scholar
  72. Zhu T, Yang C, Wang J, Zeng S, Liu M, Yang J, Bai B, Cao J, Chen X, Müller C (2018) Bacterivore nematodes stimulate soil gross N transformation rates depending on their species. Biol Fertil Soils 54:107–118CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Yuanhu Shao
    • 1
    • 2
  • Weixin Zhang
    • 1
    • 2
  • Nico Eisenhauer
    • 3
    • 4
  • Tao Liu
    • 2
    • 5
  • Olga Ferlian
    • 3
    • 4
  • Xiaoli Wang
    • 6
  • Yanmei Xiong
    • 7
  • Chenfei Liang
    • 8
  • Shenglei Fu
    • 1
    • 2
    Email author
  1. 1.Key Laboratory of Geospatial Technology for the Middle and Lower Yellow River Regions (Henan University), Ministry of Education, College of Environment and PlanningHenan UniversityKaifengChina
  2. 2.Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  3. 3.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  4. 4.Institute of BiologyLeipzig UniversityLeipzigGermany
  5. 5.University of the Chinese Academy of SciencesBeijingChina
  6. 6.State Key Laboratory of Plateau Ecology and Agriculture, Qinghai Academy of Animal and Veterinary SciencesQinghai UniversityXiningChina
  7. 7.Research Institute of Tropical ForestryChinese Academy of ForestryGuangzhouChina
  8. 8.Zhejiang Provincial Key Laboratory of Carbon Cycling in Forest Ecosystems and Carbon SequestrationZhejiang A & F UniversityLin’anChina

Personalised recommendations