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Ecosystems

, Volume 9, Issue 1, pp 75–83 | Cite as

Nitrogen Fixation by Termites in Tropical Forests, Thailand

  • Akinori Yamada
  • Tetsushi Inoue
  • Decha Wiwatwitaya
  • Moriya Ohkuma
  • Toshiaki Kudo
  • Atsuko Sugimoto
Article

Abstract

Nitrogen (N) fixed by termites was evaluated as a N input to decomposition processes in two tropical forests, a dry deciduous forest (DDF) and the neighboring dry evergreen forest (DEF), Thailand. A diverse group of termite species were assayed by acetylene reduction method and only the wood/litter-feeding termites were found to fix N. More intensive samplings of two abundant species, Microcerotermes crassus and Globitermes sulphureus, were done across several seasons, suggesting N fixation rates of 0.21 and 0.28 kg ha−1 y−1 by termites in the DDF and DEF, respectively. Also, estimates of asymbiotic N fixation rates were 0.75 and 3.95 kg ha−1 y−1. N fixed by termites and by asymbiotic fixers is directly supplied to decomposers breaking down dead plant material and could be a major source of their N. N fixed by termites was 7–22% of that fixed by termites and asymbiotic fixers. Although N fixed by termites is a small input compared to other inputs, this N is likely important for decomposition processes.

Keywords

acetylene reduction assay asymbiotic nitrogen fixation decomposition process litter and dead wood nitrogen fixation by termites tropical forests 

Notes

Acknowledgements

We thank the National Research Council of Thailand, the people who are working at Sakaerat Environmental Research Station, T. Johjima, Y. Hongoh, C. Boontong, S. Trakulnaleamsai, and N. Noparatnaraporn for their kind cooperation. We thank the chemical analysis section of RIKEN for the elemental analyses, M. B. Wamalwa, I. Tayasu, and two anonymous reviewers for their helpful comments on the manuscript, and A. Haraguchi and R. Araki for improving the English of the manuscript. This work was supported by Grant-in-Aid (09NP1501) for Creative Basic Research from Japan Ministry of Education, Culture, Sports, Science and Technology, and in part by grants from the Bioarchitect Research Program and the Eco Molecular Science Research Program from RIKEN. The first author (A. Y.) was also supported by a grant from the Junior Research Associate Program from RIKEN.

References

  1. Abe T. 1980. Studies on the distribution and ecological role of termites in a lowland rain-forest of West Malaysia. 4. The role of termites in the process of wood decomposition in Pasoh-Forest-Reserve. Revue d’Ecologie et de Biologie du Sol 17:23–40Google Scholar
  2. Benemann JR. 1973. Nitrogen fixation in termites. Science 181:164–5Google Scholar
  3. Bentley BL. 1984. Nitrogen fixation in termites – fate of newly fixed nitrogen. J Insect Physiol 30:653–5CrossRefGoogle Scholar
  4. Bignell DE, Eggleton P. 2000. Termites in ecosystems. In: Abe T, Bignell DE, Higashi M, Eds. Termite: evolution, society, symbioses, ecology. Dordrecht: Kluwer Academic. p 363–87Google Scholar
  5. Bignell DE, Eggleton P, Nunes L, Thomas KL. 1997. Termites as mediators of carbon fluxes in tropical forests: Budgets for carbon dioxide and methane emissions. In: Watt AD, Stork NE, Hunter MD, Eds. Forests and Insects. London: Chapman and Hall. p 109–34Google Scholar
  6. Breznak JA. 1975. Symbiotic relationships between termites and their intestinal microbiota. In: Jennings DH, Lee DL, Eds. Symbiosis: 29th Symposium of the Society for Experimental Biology. Cambridge: Cambridge University Press. p 559–80Google Scholar
  7. Breznak JA. 1982. Intestinal microbiota of termites and other xylophagous insects. Annu Rev Microbiol 36:323–43CrossRefPubMedGoogle Scholar
  8. Breznak JA, Brill WJ, Mertins JW, Coppel HC. 1973. Nitrogen fixation in termites. Nature 244:577–80CrossRefPubMedGoogle Scholar
  9. Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO, Perakis SS, Latty EF, Von Fischer JC, Elseroad A, Wasson MF. 1999. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Glob Biogeochem Cycles 13:623–45CrossRefGoogle Scholar
  10. Collins NM. 1980. The distribution of soil macro fauna on the west ridge of Gunung Mount Mulu Sarawak. Oecologia 44:263–75CrossRefGoogle Scholar
  11. Curtis AD, Waller DA. 1997. Variation in rates of nitrogen fixation in termites: response to dietary nitrogen in the field and laboratory. Physiol Entomol 22:303–9CrossRefGoogle Scholar
  12. Curtis AD, Waller DA. 1998. Seasonal patterns of nitrogen fixation in termites. Funct Ecol 12:803–7CrossRefGoogle Scholar
  13. Edwards PJ. 1982. Studies of mineral cycling in a montane rain forest in New Guinea 5. Rates of cycling in throughfall and litter fall. J Ecol 70:807–28Google Scholar
  14. Eggleton P. 2000. Global patterns of termite diversity. In: Abe T, Bignell DE, Higashi M, Eds. Termite: evolution, society, symbioses, ecology. Dordrecht: Kluwer Academic. p 25–51Google Scholar
  15. Eggleton P, Bignell DE. 1995. Monitoring the response of tropical insects to changes in the environment: troubles with termites. In: Harrington R, Stork NE, Eds. Insects in a changing environment. London: Academic Press. p 478–97Google Scholar
  16. Eggleton P, Homathevi R, Jones DT, MacDonald JA, Jeeva D, Bignell DE, Davies RG, Maryati M. 1999. Termite assemblages, forest disturbance and greenhouse gas fluxes in Sabah, East Malaysia. Philos Trans Roy Soc Lond B Biol Sci 354:1791–802Google Scholar
  17. Fittkau EJ, Klinge H. 1973. On biomass and trophic structure of the central Amazonian rain forest ecosystem. Biotropica 5:2–14Google Scholar
  18. Frey SD, Elliott ET, Paustian K, Peterson G. 2000. Fungal translocation as a mechanism of exogenous nitrogen inputs to decomposing surface residues in a no-tillage agroecosystem. Soil Biol Biochem 32:689–98CrossRefGoogle Scholar
  19. Hall JH, Matson PA. 2003. Nutrient status of tropical rain forests influences soil N dynamics after N additions. Ecol Monogr 73:107–29Google Scholar
  20. Hardy RW, Burns RC, Holsten RD. 1973. Applications of the acetylene-ethylene assay for measurement of nitrogen fixation. Soil Biol Biochem 5:47–81CrossRefGoogle Scholar
  21. Hunt HW, Ingham ER, Coleman DC, Elliott ET, Reid CPP. 1988. Nitrogen limitation of production and decomposition in prairie mountain meadow and pine forest. Ecology 69:1009–16Google Scholar
  22. Jordan CF. 1985. Nutrient Cycling in Tropical Forest Ecosystems: Principles and their Application in Management and Conservation. Chichester: John Wiley and Sons. 190 pGoogle Scholar
  23. Konaté S, Le Roux X, Verdier B, Lepage M. 2003. Effect of underground fungus-growing termites on carbon dioxide emission at the point- and landscape-scales in an African savanna. Funct Ecol 17:305–14Google Scholar
  24. Lovelock M, Obrien RW, Slaytor M. 1985. Effect of laboratory containment on the nitrogen metabolism of termites. Insect Biochem 15:503–10Google Scholar
  25. Martius C. 1994. Diversity and ecology of termites in Amazonian forests. Pedobiologia 38:407–28Google Scholar
  26. Nardi JB, Mackie RI, Dawson JO. 2002. Could microbial symbionts of arthropod guts contribute significantly to nitrogen fixation in terrestrial ecosystems? J Insect Physiol 48:751–63CrossRefPubMedGoogle Scholar
  27. Pandey S, Waller DA, Gordon AS. 1992. Variation in acetylene-reduction (nitrogen-fixation) rates in Reticulitermes spp. (Isoptera; Rhinotermitidae). VA J Sci 43:333–8Google Scholar
  28. Prestwich GD, Bentley BL, Carpenter EJ. 1980. Nitrogen sources for Neotropical nasute termites Nasutitermes ephratae and Rhynchotermes perarmatus fixation and selective foraging. Oecologia 46:397–401Google Scholar
  29. Rohrmann GF, Rossman AY. 1980. Nutrient strategies of Macrotermes ukuzii (Isoptera: Termitidae). Pedobiologia 20:61–73Google Scholar
  30. Roisin Y. 2000. Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi M, Eds. Termite: evolution, society, symbioses, ecology. Dordrecht: Kluwer Academic. p 95–119Google Scholar
  31. Schaefer DA, Whitford WG. 1981. Nutrient cycling by the subterranean termite Gnathamitermes tubiformans in a Chihuahuan desert ecosystem. Oecologia 48:277–83CrossRefGoogle Scholar
  32. Son Y. 2001. Non-symbiotic nitrogen fixation in forest ecosystems. Ecol Res 16:183–96CrossRefGoogle Scholar
  33. Strigel G, Ruhiyat D, Prayitno D, Sarmina S. 1994. Nutrient input by rainfall into secondary forests in East Kalimantan, Indonesia. J Trop Ecol 10:285–8Google Scholar
  34. Sylvester-Bradley R, Bandeira AG, de Oliveira LA. 1978. Fixação de nitrogênio (redução de acetileno) em cupins (Insecta: Isoptera) da Amazônia Central. Acta Amazonica 8:621–7Google Scholar
  35. Tayasu I, Sugimoto A, Wada E, Abe T. 1994. Xylophagous termites depending on atmospheric nitrogen. Naturwissenschaften 81:229–31CrossRefGoogle Scholar
  36. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI. 2002. Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45CrossRefGoogle Scholar
  37. Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea – How can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  38. Waller DA. 2000. Nitrogen fixation by termite symbionts. In: Triplett EW, Ed. Prokaryotic nitrogen fixation: a model system for analysis of a biological process. Wymondham: Horizon Scientific Press. p 225–36Google Scholar
  39. Waller DA, Breitenbeck GA, La Fage JP. 1989. Variation in acetylene-reduction by Coptotermes formosanus (Isoptera, Rhinotermitidae) related to nest source and termite size. Sociobiology 16:191–6Google Scholar
  40. Wood TG, Sands WA. 1978. The role of termites in ecosystems. In: Brian MV, Ed. Production ecology of ants and termites. Cambridge: Cambridge University Press. p 245–92Google Scholar
  41. Yamada A, Inoue T, Sugimoto A, Takematsu Y, Kumai T, Hyodo F, Fujita A, Tayasu I, Klangkaew C, Kirtibutr N, Kudo T, Abe T. 2003. Abundance and biomass of termites (Insecta: Isoptera) in dead wood in a dry evergreen forest in Thailand. Sociobiology 42:569–85Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Akinori Yamada
    • 1
    • 2
    • 7
  • Tetsushi Inoue
    • 3
    • 4
  • Decha Wiwatwitaya
    • 5
  • Moriya Ohkuma
    • 1
    • 3
    • 4
  • Toshiaki Kudo
    • 1
    • 3
    • 6
  • Atsuko Sugimoto
    • 2
    • 8
  1. 1.Environmental Molecular Biology LaboratoryRIKENWakoJapan
  2. 2.Center for Ecological ResearchKyoto UniversityShigaJapan
  3. 3.JST Bio-Recycle ProjectKasetsart University Research and Development Institute (KURDI)BangkokThailand
  4. 4.Japan Science and Technology AgencyKawaguchiJapan
  5. 5.Faculty of ForestryKasetsart UniversityBangkokThailand
  6. 6.Division of Environmental Molecular BiologyGraduate School of Integrated Science, Yokohama City UniversityYokohamaJapan
  7. 7.Center of Molecular BiosciencesUniversity of the RyukyusNishiharaJapan
  8. 8.Graduate School of Environmental Earth ScienceHokkaido UniversitySapporoJapan

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