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Nitrogen Mineralization, Ammonia Accumulation, and Emission of Gaseous NH3 by Soil-feeding Termites

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Abstract

There are numerous reports on the accumulation of ammonia in the mounds of soil-feeding termites. Here, we provided direct evidence for an effective mineralization of nitrogenous soil organic matter in the gut of Cubitermes spp., which gives rise to enormous ammonia concentrations in the intestinal tract. In Cubitermes ugandensis, the ammonia content of the nest material [24.5 μmol (g dry wt.)−1] was about 300-fold higher than that of the parent soil. Large amounts of ammonia were present throughout the intestinal tract, with lowest values in the extremely alkaline gut sections (pH >12) and highest values posterior hindgut [185 μmol (g dry wt.)−1]. Results obtained with other Cubitermes species were similar. Ammonia concentrations in the posterior hindgut of these humivorous species (up to 130 mM) are among the highest values ever reported for soil macroinvertebrates and are matched only by insects feeding on an extremely protein-rich diet (e.g., the sarcophageous larvae of blowflies). Volatilization of ammonia [about 10 nmol (g fresh wt.)−1 h−1], either directly by emission from the termite body or indirectly from their feces, led to NH3 concentrations in the nest atmosphere of C. ugandensis that were three orders of magnitude above the ambient background – a relative accumulation that is considerably higher than that observed with CH4 and CO2. Together with previous results, these observations document that through their feeding activity and due to the physicochemical and biochemical properties of their digestive system, soil-feeding termites effectively catalyze the transformation of refractory soil organic nitrogen to a plant-available form that is protected from leaching by adsorption to the nest soil. Nitrogen mineralization rates of soil-feeding termites may surpass those effected by tropical earthworms and should contribute significantly to nitrogen fluxes in tropical ecosystems.

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References

  • D.E. Bignell (1994) Soil-feeding and gut morphology in higher termites J.H. Hunt C.A. Nalepa (Eds) Nourishment and Evolution in Insect Societies Westview Press Boulder 131–158

    Google Scholar 

  • D.E. Bignell H. Oskarsson J.M. Anderson P. Ineson (1983) ArticleTitleStructuremicrobial associations and function of the so-called ‘mixed segment’ of the gut in two soil-feeding termites, Procubitermes aburiensis and Cubitermes severus (TermitidaeTermitinae) J. Zool., London. 201 445–480 Occurrence Handle10.1111/j.1469-7998.1983.tb05070.x

    Article  Google Scholar 

  • A.M. Blackmer (2000) Bioavailability of nitrogen M.E. Sumner (Eds) Handbook of Soil Science CRC Press Boca Raton D3–D18

    Google Scholar 

  • P.L. Bodelier P. Roslev T. Henckel P. Frenzel (2000) ArticleTitleStimulation by ammonium-based fertilizers of methane oxidation in soil around rice roots Nature 403 421–424 Occurrence Handle10.1038/35000193

    Article  Google Scholar 

  • U. Bosse P. Frenzel R. Conrad (1993) ArticleTitleInhibition of methane oxidation by ammonium in the surface layer of a littoral sediment FEMS Microbiol. Ecol. 13 123–134

    Google Scholar 

  • 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 

  • A. Brauman D.E. Bignell I. Tayasu (2000) Soil-feeding termites: biology, microbial associations and digestive mechanisms T. Abe D.E. Bignell M. Higashi (Eds) Termites: Evolution, Sociality, Symbiosis, Ecology Kluwer Academic Publishers Dordrecht 233–259

    Google Scholar 

  • J.A. Breznak (2000) Ecology of prokaryotic microbes in the guts of wood- and litter-feeding termites T. Abe D.E. Bignell M. Higashi (Eds) Termites: Evolution, Sociality, Symbiosis, Ecology Kluwer Academic Publishers Dordrecht 209–231

    Google Scholar 

  • A.W. Bristow (1991) ArticleTitleThe measurement of low concentrations of ammonia in the atmosphere by flow-injection analysis Commun. Soil Sci. Plant Anal. 22 1741–1752 Occurrence Handle10.1080/00103629109368532

    Article  Google Scholar 

  • A. Brune M. Kühl (1996) ArticleTitlepH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes J. Insect Physiol. 42 1121–1127 Occurrence Handle10.1016/S0022-1910(96)00036-4

    Article  Google Scholar 

  • N.M. Collins (1989) Termites H. Leith M.J.A. Werger (Eds) Ecosystems of the World: Tropical Rain Forest Ecosystems Elsevier Amsterdam 455–472

    Google Scholar 

  • S.E. Donovan P. Eggleton D.E. Bignell (2001a) ArticleTitleGut content analysis and a new feeding group classification of termites Ecol. Entomol. 26 356–366 Occurrence Handle10.1046/j.1365-2311.2001.00342.x

    Article  Google Scholar 

  • S.E. Donovan P. Eggleton W.E. Dubbin M. Batchelder L. Dibog (2001b) ArticleTitleThe effect of a soil-feeding termiteCubitermes fungifaber (IsopteraTermitidae) on soil properties: termites may be an important source of soil microhabitat heterogeneity in tropical forests Pedobiologia 45 1–11 Occurrence Handle10.1078/0031-4056-00063

    Article  Google Scholar 

  • C.A. Edwards P.J. Bohlen (1996) Biology and Ecology of Earthworms. Chapter 8: The role of earthworms in organic matter and nutrient cycles Chapman & Hall London 155–180

    Google Scholar 

  • P. Eggleton I. Tayasu (2001) ArticleTitleFeeding groups, life types and the global ecology of termites Ecol. Res. 16 941–960 Occurrence Handle10.1046/j.1440-1703.2001.00444.x

    Article  Google Scholar 

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

    Article  Google Scholar 

  • S. Fall S. Nazaret J.L. Chotte A. Brauman (2004) ArticleTitleBacterial density and community structure associated with aggregate size fractions of soil-feeding termite mounds Microb. Ecol. 48 111–199 Occurrence Handle10.1007/s00248-003-1047-2

    Article  Google Scholar 

  • E. Garnier-Sillam M. Harry (1995) ArticleTitleDistribution of humic compounds in mounds of some soil-feeding termite species of tropical rain forests: its influence on soil structure stability Insect. Soc. 42 167–185 Occurrence Handle10.1007/BF01242453

    Article  Google Scholar 

  • P.Q.J. Hall R.C. Aller (1992) ArticleTitleRapidsmall-volumeflow injection analysis for CO2NH4 + in marine and freshwaters Limnol. Oceanogr. 37 1113–1119 Occurrence Handle10.4319/lo.1992.37.5.1113

    Article  Google Scholar 

  • R. Ji A. Brune (2001) ArticleTitleTransformation and mineralization of 14C-labeled bacterial cells, protein, peptidoglycan, and cellulose by soil-feeding termites Biol. Fertil. Soils 33 166–174 Occurrence Handle10.1007/s003740000310

    Article  Google Scholar 

  • R. Ji A. Brune (2005) ArticleTitleDigestion of peptidic residues in humic substances by an alkali-stable and humic-acid-tolerant proteolytic activity in the gut of soil-feeding termites Soil Biol. Biochem. 37 1648–1655 Occurrence Handle10.1016/j.soilbio.2005.01.026

    Article  Google Scholar 

  • R. Ji A. Kappler A. Brune (2000) ArticleTitleTransformation and mineralization of synthetic 14C-labeled humic model compounds by soil-feeding termites Soil Biol. Biochem. 32 1281–1291 Occurrence Handle10.1016/S0038-0717(00)00046-8

    Article  Google Scholar 

  • A. Kappler R. Ji A. Brune (2000) ArticleTitleSynthesis and characterization of specifically 14C-labeled humic model compounds for feeding trials with soil-feeding termites Soil Biol. Biochem. 32 1271–1280 Occurrence Handle10.1016/S0038-0717(00)00047-X

    Article  Google Scholar 

  • D. Karakas S.G. Tuncel (1997) ArticleTitleOptimization and field application of a filter pack system for the simultaneous sampling of atmospheric HNO3NH3and SO2 Atmos. Environ. 31 1657–1666 Occurrence Handle10.1016/S1352-2310(96)00335-4

    Article  Google Scholar 

  • H. Knicker H.D. Lüdemann (1995) ArticleTitleN-15 and C-13 CPMAS and solution NMR studies of N-15 enriched plant material during 600 days of microbial degradation Org. Geochem. 23 329–341 Occurrence Handle10.1016/0146-6380(95)00007-2

    Article  Google Scholar 

  • H. Knicker H.D. Lüdemann K. Haider (1997) ArticleTitleIncorporation studies of NH4 + during incubation of organic residues by N-15-CPMAS-NMR-spectroscopy Eur. J. Soil Sci. 48 431–441 Occurrence Handle10.1046/j.1365-2389.1997.00093.x

    Article  Google Scholar 

  • P. Lavelle A.V. Spain (2001) Soil Ecology. Chapter 4.3: The endogeic drilosphere Kluwer Academic Publishers Dordrecht 481–494

    Google Scholar 

  • P. Lavelle M. Dangerfield C. Fragoso V. Eschenbrenner D. López-Hernández B. Pashanashi L. Brussard (1994) The relationship between soil macrofauna and tropical soil fertility O.L. Woomer M.J. Swift (Eds) The Biology Management of Tropical Soil Fertility TSBF Chichester, UK 137–169

    Google Scholar 

  • P. Lavelle D. Bignell M. Lepage V. Wolters P. Roger P. Ineson O.W. Heal S. Dhillion (1997) ArticleTitleSoil function in a changing world: the role of invertebrate ecosystem engineers Eur. J. Soil Biol. 33 159–193

    Google Scholar 

  • F.G. Lennox (1940) ArticleTitleDistribution of ammonia in larvae of Lucilia cuprina Nature 146 268

    Google Scholar 

  • X. Li A. Brune (2005a) ArticleTitleDigestion of microbial biomass, structural polysaccharides, and protein by the humivorous larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae) Soil Biol. Biochem. 37 107–116 Occurrence Handle10.1016/j.soilbio.2004.06.012

    Article  Google Scholar 

  • X. Li A. Brune (2005b) ArticleTitleSelective digestion of the peptide and polysaccharide components of synthetic humic acids by the humivorous larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae) Soil Biol. Biochem. 37 1476–1483 Occurrence Handle10.1016/j.soilbio.2005.01.004

    Article  Google Scholar 

  • D. Lopez-Hernandez (2001) ArticleTitleNutrient dynamics (C, N and P) in termite mounds of Nasutitermes ephratae from savannas of the Orinoco Llanos (Venezuela) Soil Biol. Biochem. 33 747–753 Occurrence Handle10.1016/S0038-0717(00)00220-0

    Article  Google Scholar 

  • G.M. Lovett J.E. Hart L.M. Christenson C.G. Jones (1998) ArticleTitleCaterpillar guts and ammonia volatilization: retention of nitrogen by gypsy moth larvae consuming oak foliage Oecologia (Berlin) 117 513–516 Occurrence Handle10.1007/s004420050687

    Article  Google Scholar 

  • P. Mora C. Seugé J.L. Chotte C. Rouland (2003) ArticleTitlePhysico-chemical typology of the biogenic structures of termites and earthworms: a comparative analysis Biol. Fertil. Soils 37 245–249

    Google Scholar 

  • D.E. Mullins (1974) ArticleTitleNitrogen metabolism in the American cockroach: an examination of whole body ammonium and other cations excreted in relation to water requirements J. Exp. Biol. 61 541–556

    Google Scholar 

  • D.E. Mullins D.G. Cochran (1972) ArticleTitleNitrogen excretion in cockroaches: uric acid is not a major product Science 177 699–701

    Google Scholar 

  • D.E. Mullins D.G. Cochran (1976) ArticleTitleA comparative study of nitrogen excretion in twenty-three cockroach species Comp. Biochem. Physiol. 53A 393–399

    Google Scholar 

  • K.J. Nadelhoffer B. Fry (1994) Nitrogen isotope studies in terrestrial ecosystems K. Lajtha R.H. Michener (Eds) Ecology and Environmental Science Blackwell Science Ltd Oxford 22–44

    Google Scholar 

  • D. Ndiaye R. Lensi M. Lepage A. Brauman (2004) ArticleTitleThe effect of the soil-feeding termite Cubitermes niokoloensis on soil microbial activity in a semi-arid savanna in West Africa Plant Soil 259 277–286 Occurrence Handle10.1023/B:PLSO.0000020980.50095.e1

    Article  Google Scholar 

  • C. Noirot (1992) From wood- to humus-feeding: an important trend in termite evolution J. Billen (Eds) Biology and Evolution of Social Insects Leuven University Press Leuven, Belgium 107–119

    Google Scholar 

  • J.W. Parsons (1988) Isolation of humic substances from soils and sediments F.H. Frimmel R.F. Christman (Eds) in Humic Substances and Their Role in the Environment Wiley Chichester 3–14

    Google Scholar 

  • H. Platen B. Schink (1987) ArticleTitleMethanogenic degradation of acetone by an enrichment culture Arch. Microbiol. 149 136–141 Occurrence Handle10.1007/BF00425079

    Article  Google Scholar 

  • C.J. Potrikus J.A. Breznak (1981) ArticleTitleGut bacteria recycle uric acid nitrogen in termites: A strategy for nutrient conservation Proc. Natl. Acad. Sci. USA 78 4601–4605

    Google Scholar 

  • R.D. Prusch (1971) ArticleTitleThe site of ammonia excretion in the blowfly larvaSarcophaga bullata Comp. Biochem. Physiol. 39A 761–767 Occurrence Handle10.1016/0300-9629(71)90198-8

    Article  Google Scholar 

  • W.H. Schlesinger A.E. Hartley (1992) ArticleTitleA global budget for atmospheric NH3 Biogeochemistry 15 191–211 Occurrence Handle10.1007/BF00002936

    Article  Google Scholar 

  • D. Schmitt-Wagner A. Brune (1999) ArticleTitleHydrogen profiles and localization of methanogenic activities in the highly compartmentalized hindgut of soil-feeding higher termites (Cubitermes spp.) Appl. Environ. Microbiol. 65 4490–4496

    Google Scholar 

  • D. Schmitt-Wagner M.W. Friedrich B. Wagner A. Brune (2003a) ArticleTitlePhylogenetic diversity, abundanceand axial distribution of bacteria in the intestinal tract of two soil-feeding termites (Cubitermes spp.) Appl. Environ. Microbiol. 69 6007–6017 Occurrence Handle10.1128/AEM.69.10.6007-6017.2003

    Article  Google Scholar 

  • D. Schmitt-Wagner M.W. Friedrich B. Wagner A. Brune (2003b) ArticleTitleAxial dynamics, stability, and interspecies similarity of bacterial community structure in the highly compartmentalized gut of soil-feeding termites (Cubitermes spp.) Appl. Environ. Microbiol. 69 6018–6024 Occurrence Handle10.1128/AEM.69.10.6018-6024.2003

    Article  Google Scholar 

  • S. Schnell G.M. King (1994) ArticleTitleMechanistic analysis of ammonium inhibition of atmospheric methane consumption in forest soils Appl. Environ. Microbiol. 60 3514–3521

    Google Scholar 

  • M. Schnitzer (1985) Nature of nitrogen in humic substances G.R. Aiken D.M. MacKnight R.L. Wershaw P. MacCarthy (Eds) Soil, Sediment and Water: Geochemistry, Isolation and Characterization John Wiley New York 303–325

    Google Scholar 

  • M. Slaytor D.J. Chappell (1994) ArticleTitleNitrogen metabolism in termites Comp. Biochem. Physiol. 107 1–10

    Google Scholar 

  • F. Sleaford D.E. Bignell P. Eggleton (1996) ArticleTitleA pilot analysis of gut contents in termites from the Mbalmayo Forest reserveCameroon Ecol. Entomol. 21 279–288

    Google Scholar 

  • F.J. Stevenson (1994) Humus chemistry. Genesis, Composition, Reactions EditionNumber2 John Wiley & Sons New York

    Google Scholar 

  • A. Sugimoto T. Inoue N. Kirtibutr T. Abe (1998) ArticleTitleMethane oxidation by termite mounds estimated by the carbon isotopic composition of methane Global Biogeochem. Cycles 12 595–605 Occurrence Handle10.1029/98GB02266

    Article  Google Scholar 

  • I. Tayasu T. Abe P. Eggleton D.E. Bignell (1997) ArticleTitleNitrogen and carbon isotope ratios in termites: an indicator of trophic habit along the gradient from wood-feeding to soil-feeding Ecol. Entomol. 22 343–351 Occurrence Handle10.1046/j.1365-2311.1997.00070.x

    Article  Google Scholar 

  • A. Vairavamurthy S. Wang (2002) ArticleTitleOrganic nitrogen in geomacromolecules: insights on speciation and transformation with K-edge XANES spectroscopy Environ. Sci. Technol. 36 3050–3056 Occurrence Handle10.1021/es0155478

    Article  Google Scholar 

  • T.G. Wood (1978) The role of termites (Isoptera) in decomposition processes J.M. Anderson A. Macfadyen (Eds) The Role of Terrestrial and Aquatic Organisms in Decomposition Processes Blackwell Oxford 145–168

    Google Scholar 

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

    Article  Google Scholar 

  • T.G. Wood (1996) The agricultural importance of termites in the tropics K. Evans (Eds) Agricultural Zoology Reviews NumberInSeriesVol. 7 Intercept Andover 117–155

    Google Scholar 

  • P.A. Wright (1995) ArticleTitleNitrogen excretion: three end products, many physiological roles J. Exp. Biol. 198 273–281

    Google Scholar 

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JI, R., Brune, A. Nitrogen Mineralization, Ammonia Accumulation, and Emission of Gaseous NH3 by Soil-feeding Termites. Biogeochemistry 78, 267–283 (2006). https://doi.org/10.1007/s10533-005-4279-z

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