Skip to main content

Advertisement

Log in

Bacterial Density and Community Structure Associated with Aggregate Size Fractions of Soil-Feeding Termite Mounds

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The building and foraging activities of termites are known to modify soil characteristics such as the heterogeneity. In tropical savannas the impact of the activity of soil-feeding termites (Cubitermes niokoloensis) has been shown to affect the properties of the soil at the aggregate level by creating new soil microenvironments (aggregate size fractions) [13]. These changes were investigated in greater depth by looking at the microbial density (AODC) and the genetic structure (automated rRNA intergenic spacer analysis: ARISA) of the communities in the different aggregate size fractions (i.e., coarse sand, fine sand, coarse silt, fine silt, and dispersible clays) separated from compartments (internal and external wall) of three Cubitermes niokoloensis mounds. The bacterial density of the mounds was significantly higher (1.5 to 3 times) than that of the surrounding soil. Within the aggregate size fractions, the termite building activity resulted in a significant increase in bacterial density within the coarser fractions (>20 μm). Multivariate analysis of the ARISA profiles revealed that the bacterial genetic structures of unfractionated soil and soil aggregate size fractions of the three mounds was noticeably different from the savanna soil used as a reference. Moreover, the microbial community associated with the different microenvironments in the three termite mounds revealed three distinct clusters formed by the aggregate size fractions of each mound. Except for the 2–20 μm fraction, these results suggest that the mound microbial genetic structure is more dependent upon microbial pool affiliation (the termite mound) than on the soil location (aggregate size fraction). The causes of the specificity of the microbial community structure of termite mound aggregate size fractions are discussed.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. JM Anderson TG Wood (1984) ArticleTitleMound composition and soil modification by two soil feeding termites (Termitinae, termitidae). Pedobiology 26 77–82

    Google Scholar 

  2. DE Bignell JM Anderson R Crosse (1991) ArticleTitleIsolation of facultatively aerobic actinomycetes from the gut, parent soil and mound materials of the termites Procubitermes aburiensis and Cubitermes severus. FEMS Microbiol Ecol 85 151–160 Occurrence Handle10.1016/0378-1097(91)90511-8

    Article  Google Scholar 

  3. DE Bignell P Eggleton (1995) ArticleTitleOn the elevated intestinal pH of higher termites (Isoptera: Termitidae). Ins Soc 42 57–69

    Google Scholar 

  4. A Brauman (2000) ArticleTitleEffect of gut transit and mound deposit on soil organic matter transformations in the soil feeding termite: A review. Eur J Soil Biol 36 117–125 Occurrence Handle10.1016/S1164-5563(00)01058-X

    Article  Google Scholar 

  5. A Brauman DE Bignell I Tayasu (2000) Soil-feeding termites: biology, microbial associations and digestive mechanisms. T Abe DE Bignell M Higashi (Eds) Termites: Evolution, Sociality, Symbioses, Ecology, vol. 2 Kluwer Academic Dordrecht 233–259

    Google Scholar 

  6. A Brune (1998) ArticleTitleTermite gut: the world’s smallest bioreactor. Trends Biotechnol 16 16–21 Occurrence Handle10.1016/S0167-7799(97)01151-7 Occurrence Handle1:CAS:528:DyaK1cXnt1Siuw%3D%3D

    Article  CAS  Google Scholar 

  7. A Brune D Emerson JA Breznack (1995) ArticleTitleThe termites gut microflora as an oxygen sink: Microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl Environ Microbiol 61 2681–2687 Occurrence Handle1:CAS:528:DyaK2MXms1Grsrg%3D

    CAS  Google Scholar 

  8. A Brune M Friedrich (2000) ArticleTitleMicroecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3 263–269 Occurrence Handle10.1016/S1369-5274(00)00087-4 Occurrence Handle1:STN:280:DC%2BD3czhtFGjsA%3D%3D Occurrence Handle10851155

    Article  CAS  PubMed  Google Scholar 

  9. JL Chotte JN Ladd M Amato (1998) ArticleTitleSites of microbial assimilation and turnover of soluble and particulate C-labelled substrates decomposing in a clay soil. Soil Biol Biochem 30 205–218 Occurrence Handle10.1016/S0038-0717(97)00115-6 Occurrence Handle1:CAS:528:DyaK1cXnslCrtQ%3D%3D

    Article  CAS  Google Scholar 

  10. JL Chotte A Schwartzmann R Bally L Jocteur-Monrozier (2002) ArticleTitleChanges in bacterial communities and Azospirillum diversity in soil fractions of a tropical soil under 3 and 19 years of natural fallow. Soil Biol Biochem 34 1083–1092 Occurrence Handle10.1016/S0038-0717(02)00041-X Occurrence Handle1:CAS:528:DC%2BD38Xlt1Oisbc%3D

    Article  CAS  Google Scholar 

  11. P Eggleton DE Bignell WA Sands B Waite TG Wood JH Lawton (1995) ArticleTitleThe species richness of termites (Isptera) under differing levels of forest disturbance in the Mbalmayo Forest Reserve, Southern Cameroon. J Trop Ecol 11 85–98

    Google Scholar 

  12. S Fall A Brauman JL Chotte (2001) ArticleTitleComparative distribution of organic matter in particle and aggregate size fraction in the mounds of with different feeding habitats in Senegal: Cubitermes niokoloensis and Macrotermes bellicosus. Appl Soil Ecol 17 131–140 Occurrence Handle10.1016/S0929-1393(01)00125-1

    Article  Google Scholar 

  13. M Fisher EW Triplett (1999) ArticleTitleAutomated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65 4630–4636

    Google Scholar 

  14. E Garnier-Sillam M Harry (1995) ArticleTitleDistribution of humic compounds in mounds of soil feeding termites: its influence on soil structural stability. Ins Soc 42 167–185

    Google Scholar 

  15. E Garnier-Sillam F Toutain J Renoux (1988) ArticleTitleComparaison de I’influence de deux termitières (humivore et champignonniste) sur la stabilité structurale des sols forestiers tropicaux. Pedobiology 32 89–97

    Google Scholar 

  16. M Harry N Jusseaume B Gambier E Garnier-Sillam (2001) ArticleTitleUse of RAPD markers for the study of microbial community similarity from termite mounds and tropical soils. Soil Biol Biochem 33 417–427 Occurrence Handle10.1016/S0038-0717(00)00181-4 Occurrence Handle1:CAS:528:DC%2BD3MXis1aksr8%3D

    Article  CAS  Google Scholar 

  17. JE Hobbie RJ Daley S Jasper (1977) ArticleTitleUse of Nuclepore filters for counting bacteria by fluorescence Microscopy. Appl Environ Microbiol 33 1225–1228 Occurrence Handle1:STN:280:CSiB38%2FjvVE%3D Occurrence Handle327932

    CAS  PubMed  Google Scholar 

  18. JA Holt M Lepage (2000) Termites and soil properties. T Abe DE Bignell M Higashi (Eds) Termites: Evolution, Sociality, Symbioses, Ecology, vol. 2 Kluwer Academic Dordrecht 389–407

    Google Scholar 

  19. R Ji A Brune (2001) ArticleTitleTransformation and mineralization of 14C-labeled bacterial cells, protein, peptidoglycan, and cellulose by soil-feeding ermites. Biol Fertil Soils 33 166–174 Occurrence Handle10.1007/s003740000310 Occurrence Handle1:CAS:528:DC%2BD3MXmvFGluw%3D%3D

    Article  CAS  Google Scholar 

  20. CG Jones JH Lawton M Shachak (1994) ArticleTitleOrganisms as ecosystem engineers. Oikos 69 373–386

    Google Scholar 

  21. CG Jones JH Lawton M Shachak (1997) ArticleTitlePositive and negative effects of organisms as physical ecosystem engineers. Ecology 78 1946–1957

    Google Scholar 

  22. S Kanazawa Z Filip (1986) ArticleTitleDistribution of microorganisms, total biomass, and enzyme activities in different particles of brown soil. Microb Ecol 12 205–215 Occurrence Handle1:CAS:528:DyaL28XksFOmtL8%3D

    CAS  Google Scholar 

  23. E Kandeler S Pallia M Stemmera MH Gerzabekb (1999) ArticleTitleTillage changes microbial biomass and enzyme activities in particle-size fractions of a Haplic Chernozem. Soil Biol Biohem 31 1253–1264 Occurrence Handle10.1016/S0038-0717(99)00041-3 Occurrence Handle1:CAS:528:DyaK1MXktlyjurc%3D

    Article  CAS  Google Scholar 

  24. E Kandeler D Tscherko KD Bruce M Stemmer PJ Hobbs RD Bardgett W Amelung (2000) ArticleTitleStructure and function of the soil microbial community in microhabitats of a heavy metal polluted soil. Biol Fertil Soils 32 390–400 Occurrence Handle10.1007/s003740000268 Occurrence Handle1:CAS:528:DC%2BD3cXosVSjtLY%3D

    Article  CAS  Google Scholar 

  25. E Kandeler D Tscherko M Stemmer S Schwarz H Gerzabek (2001) ArticleTitleOrganic matter and soil microorganisms-Investigations from the micro- and the macro-scale. Austrian J Agric Res 52 25–31

    Google Scholar 

  26. A Kappler A Brune (1999) ArticleTitleInfluence of gut alkalinity and oxygen status on mobilisation and size-class distribution of humic acids in the hindgut of soil-feeding termites. Appl Soil Ecol 13 219–229 Occurrence Handle10.1016/S0929-1393(99)00035-9

    Article  Google Scholar 

  27. P Lavelle (2000) ArticleTitleEcological challenges for soil science. Soil Sci 165 73–86 Occurrence Handle10.1097/00010694-200001000-00009 Occurrence Handle1:CAS:528:DC%2BD3cXhtFCgt7s%3D

    Article  CAS  Google Scholar 

  28. P Lavelle D Bignell M Lepage V Wolters P Roger P Ineson OW Heal S Dhillion (1997) ArticleTitleSoil function in a changing world: the role of invertebrate ecosystem engineers. Eur J Soil Biol 33 159–193 Occurrence Handle1:CAS:528:DyaK1cXmvVWnsro%3D

    CAS  Google Scholar 

  29. KE Lee TG Wood (1971) Termite and Soil Academic Press London

    Google Scholar 

  30. R Lensi A Clays-Josser LJ Monrozier (1995) ArticleTitleDenitrifiers and denitrifying activity in size fractions of a mollisol under permanent pasture and continuous cultivation. Soil Biol Biochem 27 61–69 Occurrence Handle10.1016/0038-0717(94)00132-K Occurrence Handle1:CAS:528:DyaK2MXjtFOisLY%3D

    Article  CAS  Google Scholar 

  31. RJ Manlay P Cadet J Thioulouse JL Chotte (2000) ArticleTitleRelationship between abiotic and biotic soil properties during fallow periods in the sudanian zone of Senegal. Appl Soil Ecol 14 89–101 Occurrence Handle10.1016/S0929-1393(00)00052-4

    Article  Google Scholar 

  32. LJ Monrozier JN Ladd RW Fitzpatrick RC Foster M Raupach (1991) ArticleTitleComponent and microbial biomass content of size fractions in soil contrasting aggregates. Geoderma 49 37–62 Occurrence Handle10.1016/0016-7061(91)90025-O

    Article  Google Scholar 

  33. C Noirot JPEC Darlington (2000) Termite nest: architecture, regulation and defence. T Abe DE Bignell M Higashi (Eds) Termites: Evolution, Sociality, Symbioses, Ecology, vol. 2 Kluwer Academic Dordrecht 121–139

    Google Scholar 

  34. P Normand C Ponsonnet X Nesme M Neyra P Simonet (1996) ITS analysis of prokaryotes. DL Akkermans JD Van Elsas EI de Bruijn (Eds) Molecular Microbial Ecology Manual Kluwer Academic Publishers Amsterdam 1–12

    Google Scholar 

  35. LA Porteous RJ Seidler LS Watrud (1997) ArticleTitleAn improved method for purifying DNA from soil for PCR amplification and molecular ecology applications. Mol Ecol 6 787–791 Occurrence Handle10.1046/j.1365-294X.1997.00241.x Occurrence Handle1:CAS:528:DyaK2sXls1WrsLc%3D

    Article  CAS  Google Scholar 

  36. L Ranjard F Poly J Combrisson A Richaume F Gourbière J Thioulouse S Nazaret (2000) ArticleTitleHeterogeneous cell density and genetic structure of bacterial pools associated with various soil microenvironment as determined by enumeration and DNA fingerprinting approach (RISA). Microb Ecol 39 263–272 Occurrence Handle1:CAS:528:DC%2BD3cXlsFGhtLc%3D Occurrence Handle10882431

    CAS  PubMed  Google Scholar 

  37. L Ranjard F Poly JC Lata C Mougel J Thioulouse S Nazaret (2001) ArticleTitleCharacterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprinting: biological and methodological variability. Appl Environ Microbiol 67 4479–4487

    Google Scholar 

  38. A Richaume C Steinberg LJ Monrozier G Faurie (1993) ArticleTitleDifference between direct and indirect enumeration of soil bacteria: influence of soil structure and cell location. Soil Biol Biochem 25 641–643 Occurrence Handle10.1016/0038-0717(93)90206-Q

    Article  Google Scholar 

  39. SN Sall A Brauman S Fall C Rouland E Miambi JL Chotte (2002) ArticleTitleVariation in the distribution of monosaccharides in soil fractions in the mounds of termites with different feeding habits (Senegal). Biol Fertil Soils 36 232–239 Occurrence Handle10.1007/s00374-002-0515-z Occurrence Handle1:CAS:528:DC%2BD38XntlOmtLo%3D

    Article  CAS  Google Scholar 

  40. M Sarr C Agbogba A Russell-Smith (1998) ArticleTitleThe effects of length of fallow and cultivation on termite abundance and diversity in the sahelian zone of Senegal: a preliminary note. Pedobiol 42 56–62

    Google Scholar 

  41. A Sessitsch A Weilharter MH Gerzabek H Kirchmann E Kandeler (2001) ArticleTitleMicrobial population structures in soil particle size fraction of a long-term fertilizer field experiment. Appl Environ Microbiol 67 4215–4224

    Google Scholar 

  42. F Sleaford DE Bignell P Eggleton (1996) ArticleTitleA pilot analysis of gut contents in termites from the Mbalmayo forest reserve, Cameroun. Ecol Entomol 21 279–288

    Google Scholar 

  43. J Thioulouse D Chesse S Dolédec JM Olivier (1997) ArticleTitleADE-4: a multivariate analysis and graphical display software. Stat Comput 7 75–83 Occurrence Handle10.1023/A:1018513530268

    Article  Google Scholar 

  44. A Winding R Ronn NB Hendriksen (1997) ArticleTitleBacteria and protozoa in soil microhabits as affected by earthworms. Biol Fertil Soils 24 133–140 Occurrence Handle10.1007/s003740050221

    Article  Google Scholar 

  45. TG Wood (1988) ArticleTitleTermites and the soil environment. Biol Fertil Soils 6 228–236 Occurrence Handle10.1007/BF00260819

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported financially by the CNRS French Biodiversity Institute Environmental Life and Society program and by the French Institute for Research and Development (IRD, ex-ORSTOM). We thank Lamine Dieng and Ndeye Fatou Dieng for their technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Brauman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fall, S., Nazaret, S., Chotte, J. et al. Bacterial Density and Community Structure Associated with Aggregate Size Fractions of Soil-Feeding Termite Mounds. Microb Ecol 48, 191–199 (2004). https://doi.org/10.1007/s00248-003-1047-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-003-1047-2

Keywords

Navigation