Advertisement

Microbial Ecology

, Volume 63, Issue 4, pp 905–918 | Cite as

Protozoan Pulses Unveil Their Pivotal Position Within the Soil Food Web

  • Felicity V. CrottyEmail author
  • Sina M. Adl
  • Rod P. Blackshaw
  • Philip J. Murray
Invertebrate Microbiology

Abstract

Protozoa are one of the most abundant groups of bacterivores within the soil and are responsible for mineralisation of bacterial biomass, having a large impact on C and N cycling. Little is known of their contribution to soil nutrient transfers or the identity of their consumers. Here, for the first time indigenous flagellates and ciliates, enriched to 83 atom% for 13C and 10 atom% for 15N, were introduced to soil cores from two different land managements, grassland and woodland with the same soil type, to trace the flow of protozoan C and N through the soil food web. Nematodes, Collembola, earthworms and insect larvae obtained the greatest amounts of C and N of protozoan origin, either through direct consumption or uptake of biomass post-cell death. Our results show that changes in management, affect the functioning of the soil food web and the utilisation of protozoa as a food source.

Keywords

Stable Isotope Soil Respiration Soil Core Natural Abundance Gini Coefficient 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The authors would like to thank Dan Dhanoa for statistical advice, Dr. Barry Thornton at the Macaulay Institute (UKAS accredited laboratory) for operation of the elemental analyser linked to an isotope ratio mass spectrometer and Liz Dixon at Rothamsted Research, North Wyke, for operation of the trace gas analyser linked to a mass spectrometer. Rothamsted Research is sponsored by the UK Biotechnology and Biological Sciences Research Council. This work was carried out as part of a BBSRC DTG studentship.

References

  1. 1.
    Adl MS, Gupta V (2006) Protists in soil ecology and forest nutrient cycling. Can J For Res-Rev Can Rech For 36:1805–1817CrossRefGoogle Scholar
  2. 2.
    Adl MS, Acosta-Mercado D, Anderson RT, Lynn HD (2007) Protozoa, supplementary material. In: Carter MR, Gregorich EG (eds) Soil sampling and methods of analysis, chapter 36. CRC Press, Boca Raton, p 1264Google Scholar
  3. 3.
    Adl SM (2003) The ecology of soil decomposition. CABI Publishing, WallingfordCrossRefGoogle Scholar
  4. 4.
    Adl SM, Coleman DC (2005) Dynamics of soil protozoa using a direct count method. Biol Fertil Soils 42:168–171CrossRefGoogle Scholar
  5. 5.
    Bardgett RD (2005) The biology of soil: a community and ecosystem approach. Oxford University Press, New YorkGoogle Scholar
  6. 6.
    Bardgett RD, Leemans DK, Cook R, Hobbs PJ (1997) Seasonality of the soil biota of grazed and ungrazed hill grasslands. Soil Biol Biochem 29:1285–1294CrossRefGoogle Scholar
  7. 7.
    Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631CrossRefGoogle Scholar
  8. 8.
    Bonkowski M, Griffiths B, Scrimgeour C (2000) Substrate heterogeneity and microfauna in soil organic ‘hotspots’ as determinants of nitrogen capture and growth of ryegrass. Appl Soil Ecol 14:37–53CrossRefGoogle Scholar
  9. 9.
    Brussaard L, Behan-Pelletier VM, Bignell DE, Brown VK, Didden W, Folgarait P, Fragoso C, Freckman DW, Gupta V, Hattori T, Hawksworth DL, Klopatek C, Lavelle P, Malloch DW, Rusek J, Soderstrom B, Tiedje JM, Virginia RA (1997) Biodiversity and ecosystem functioning in soil. Ambio 26:563–570Google Scholar
  10. 10.
    Chahartaghi M, Langel R, Scheu S, Ruess L (2005) Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biol Biochem 37:1718–1725CrossRefGoogle Scholar
  11. 11.
    Coleman DC (1994) The microbial loop concept as used in terrestrial soil ecology studies. Microb Ecol 28:245–250CrossRefGoogle Scholar
  12. 12.
    Crotty FV, Blackshaw RP, Murray PJ (2011) Differential growth of the fungus Absidia cylindrospora on 13C/15N-labelled media. Rapid Commun Mass Spectrom 25:1479–1484PubMedCrossRefGoogle Scholar
  13. 13.
    Crotty FV, Blackshaw RP, Murray PJ (2011) Tracking the flow of bacterially derived 13C and 15N through soil faunal feeding channels. Rapid Commun Mass Spectrom 25:1503–1513PubMedCrossRefGoogle Scholar
  14. 14.
    De Ruiter PC, Vanveen JA, Moore JC, Brussaard L, Hunt HW (1993) Calculation of nitrogen mineralization in soil food webs. Plant Soil 157:263–273CrossRefGoogle Scholar
  15. 15.
    Deharveng L (2004) Recent advances in Collembola systematics. Pedobiologia 48:415–433CrossRefGoogle Scholar
  16. 16.
    Dyckmans J, Scrimgeour CM, Schmidt O (2005) A simple and rapid method for labelling earthworms with 15N and 13C. Soil Biol Biochem 37:989–993CrossRefGoogle Scholar
  17. 17.
    Ekelund F, Rønn R, Griffiths BS (2001) Quantitative estimation of flagellate community structure and diversity in soil samples. Protist 152:301–314PubMedCrossRefGoogle Scholar
  18. 18.
    Elfstrand S, Lagerlöf J, Hedlund K, Mårtensson A (2008) Carbon routes from decomposing plant residues and living roots into soil food webs assessed with 13C labelling. Soil Biol Biochem 40:2530–2539CrossRefGoogle Scholar
  19. 19.
    Esteban GF, Clarke KJ, Olmo JL, Finlay BJ (2006) Soil protozoa-an intensive study of population dynamics and community structure in an upland grassland. Appl Soil Ecol 33:137–151CrossRefGoogle Scholar
  20. 20.
    Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183CrossRefGoogle Scholar
  21. 21.
    Fabian M (1998) The effects of different methods of preservation on the 15N concentration in Folsomia candida (Collembola). Appl Soil Ecol 9:101–104CrossRefGoogle Scholar
  22. 22.
    Hakvoort SGH, Schmidt O (2002) 15N stable isotope labelling of slugs (Gastropoda: Pulmonata). Ann Appl Biol 141:275–281CrossRefGoogle Scholar
  23. 23.
    Halaj J, Peck RW, Niwa CG (2005) Trophic structure of a macroarthropod litter food web in managed coniferous forest stands: a stable isotope analysis with δ15N and δ13C. Pedobiologia 49:109–118CrossRefGoogle Scholar
  24. 24.
    Harrod TR, Hogan DV (2008) The soils of North Wyke and Rowden. In: Soil survey of England and Wales. Rothamsted Research, OkehamptonGoogle Scholar
  25. 25.
    Hatch DJ, Jarvis SC, Parkinson RJ, Lovell RD (2000) Combining field incubation with nitrogen-15 labelling to examine nitrogen transformations in low to high intensity grassland management systems. Biol Fertil Soils 30:492–499CrossRefGoogle Scholar
  26. 26.
    Hopkin SP (1997) Biology of springtails. Oxford University Press, OxfordGoogle Scholar
  27. 27.
    Hunt HW, Coleman DC, Ingham ER, Ingham RE, Elliott ET, Moore JC, Rose SL, Reid CPP, Morley CR (1987) The detrital food web in a shortgrass prairie. Biol Fertil Soils 3:57–68CrossRefGoogle Scholar
  28. 28.
    Illig J, Langel R, Norton RA, Scheu S, Maraun M (2005) Where are the decomposers? Uncovering the soil food web of a tropical montane rain forest in southern Ecuador using stable isotopes (15N). J Trop Ecol 21:589–593CrossRefGoogle Scholar
  29. 29.
    Janssen MPM, Heijmans G (1998) Dynamics and stratification of protozoa in the organic layer of a scots pine forest. Biol Fertil Soils 26:285–292CrossRefGoogle Scholar
  30. 30.
    Jorgensen HB, Elmholt S, Petersen H (2003) Collembolan dietary specialisation on soil grown fungi. Biol Fertil Soils 39:9–15CrossRefGoogle Scholar
  31. 31.
    Knohl A, Werner RA, Geilmann H, Brand WA (2004) Kel-f (tm) discs improve storage time of canopy air samples in 10-ml vials for CO2 δ 13C analysis. Rapid Commun Mass Spectrom 18:1663–1665PubMedCrossRefGoogle Scholar
  32. 32.
    Koehler HH (1999) Predatory mites (Gamasina, Mesostigmata). Agric Ecosyst Environ 74:395–410CrossRefGoogle Scholar
  33. 33.
    Krantz GW, Walter DE (2009) A manual of acarology. Texas Tech University Press, TexasGoogle Scholar
  34. 34.
    Leake JR, Ostle NJ, Rangel-Castro JI, Johnson D (2006) Carbon fluxes from plants through soil organisms determined by field (CO2)-13C pulse-labelling in an upland grassland. Appl Soil Ecol 33:152–175CrossRefGoogle Scholar
  35. 35.
    Midwood AJ, Gebbing T, Wendler R, Sommerkorn M, Hunt JE, Millard P (2006) Collection and storage of CO2 for 13C analysis: An application to separate soil CO2 efflux into root-and soil-derived components. Rapid Commun Mass Spectrom 20:3379–3384PubMedCrossRefGoogle Scholar
  36. 36.
    Moore JC, Walter DE, Hunt HW (1988) Arthropod regulation of microbiota and mesobiota in belowground detrital food webs. Annu Rev Entomol 33:419–439CrossRefGoogle Scholar
  37. 37.
    Moore JC, McCann K, de Ruiter PC (2005) Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiologia 49:499–510CrossRefGoogle Scholar
  38. 38.
    Murray PJ, Clegg CD, Crotty FV, de la Fuente MN, Williams JK, Blackshaw RP (2009) Dissipation of bacterially derived C and N through the meso-and macrofauna of a grassland soil. Soil Biol Biochem 41:1146–1150CrossRefGoogle Scholar
  39. 39.
    Osler GHR, Sommerkorn M (2007) Toward a complete soil C and N cycle: Incorporating the soil fauna. Ecology 88:1611–1621PubMedCrossRefGoogle Scholar
  40. 40.
    Ostle N, Briones MJI, Ineson P, Cole L, Staddon P, Sleep D (2007) Isotopic detection of recent photosynthate carbon flow into grassland rhizosphere fauna. Soil Biol Biochem 39:768–777CrossRefGoogle Scholar
  41. 41.
    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
  42. 42.
    Pokarzhevskii AD, van Straalen NM, Zaboev DP, Zaitsev AS (2003) Microbial links and element flows in nested detrital food-webs. Pedobiologia 47:213–224CrossRefGoogle Scholar
  43. 43.
    Pollierer MM, Langel R, Scheu S, Maraun M (2009) Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and 13C/12C). Soil Biol Biochem 41:1221–1226CrossRefGoogle Scholar
  44. 44.
    Pollierer MM, Langel R, Korner C, Maraun M, Scheu S (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736PubMedCrossRefGoogle Scholar
  45. 45.
    Ponsard S, Amlou M (1999) Effects of several preservation methods on the isotopic content of drosophila samples. Comptes Rendus Acad Sci Ser III-Sci Vie-Life Sci 322:35–41Google Scholar
  46. 46.
    Scheu S, Falca M (2000) The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: stable isotope analysis of a macro-and a mesofauna-dominated community. Oecologia 123:285–296CrossRefGoogle Scholar
  47. 47.
    Scheu S, Simmerling F (2004) Growth and reproduction of fungal feeding Collembola as affected by fungal species, melanin and mixed diets. Oecologia 139:347–353PubMedCrossRefGoogle Scholar
  48. 48.
    Schmidt O, Scrimgeour CM (2001) A simple urea leaf-feeding method for the production of 13C and 15N labelled plant material. Plant Soil 229:197–202CrossRefGoogle Scholar
  49. 49.
    Schmidt O, Curry JP, Dyckmans J, Rota E, Scrimgeour CM (2004) Dual stable isotope analysis (δ13C and δ15N) of soil invertebrates and their food sources. Pedobiologia 48:171–180CrossRefGoogle Scholar
  50. 50.
    Sonneborn TM (1970) Methods in Paramecium research. In: Prescott DM (ed) Methods of cell physiology, vol 4. Academic, New York, pp 241–339Google Scholar
  51. 51.
    Walter DE, Ikonen EK (1989) Species, guilds, and functional groups—taxonomy and behaviour in nematophagous arthropods. J Nematol 21:315–327PubMedGoogle Scholar
  52. 52.
    Whitehead AG, Hemming JR (1965) A comparison of some quantitative methods of extracting small vermiform Nematodes from soil. Ann Appl Biol 55:25–38CrossRefGoogle Scholar
  53. 53.
    Yeates GW, Bongers T, Degoede RGM, Freckman DW, Georgieva SS (1993) Feeding-habits in soil Nematode families and genera—an outline for soil ecologists. J Nematol 25:315–331PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Felicity V. Crotty
    • 1
    • 2
    • 3
    Email author
  • Sina M. Adl
    • 3
  • Rod P. Blackshaw
    • 2
  • Philip J. Murray
    • 1
  1. 1.Sustainable Soil and Grassland SystemsRothamsted ResearchOkehamptonUK
  2. 2.School of Biomedical and Biological SciencesUniversity of PlymouthPlymouthUK
  3. 3.Faculty of ScienceDalhousie UniversityHalifaxCanada

Personalised recommendations