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Changes in amount of bacteria during gut passage of leaf litter and during coprophagy in three species ofBibionidae (Diptera) larvae

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Abstract

To elucidate the interaction between bacteria and saprophagousDiptera larvae, the amounts of bacteria in leaf litter, individual gut compartments, and feces of three species ofBibionidae (Bibio pomonae, Bibio marci, andPenthetria holosericea), feeding either directly on leaf litter or on fecal pellets produced from leaf litter by larvae of the same species, were assessed by determining total direct counts and viable counts on solid media at different pH. InP. holosericea, the effect of various cultivation temperatures on direct counts of bacteria in individual compartments was also demonstrated. In all species, the amount of bacteria in the anterior mesenteron was lower than in the consumed food, regardless of whether the larvae were feeding on leaf litter or feces, and increased again in the posterior part of the gut. The amount of bacteria in these compartments was generally higher in larvae feeding on feces than in those feeding on leaf litter, whereas the amount of bacteria found in the ceca varied. InB. marci, the amount of bacteria in the mesenteron sections able to grow on alkaline medium (pH 9) was higher than that of bacteria able to grow on slightly acidic medium (pH 5.5) during both the first and the second gut passage. InB. pomonae andP. holosericea, this increase was observed only during the second gut passage. The effect of gut passage inP. holosericea on changes in direct counts of bacteria was more pronounced when the larvae were fed at 5 °C as compared to 20 °C. Radiolabeled bacteria were digested in the gut and utilized as a source of energy and nutrients by the larvae; digested bacteria represented up to 10 % of the material assimilated by the larvae. Lysozyme activity in whole-gut extracts ofP. holosericea had a pH optimum of at pH 7, indicating a lowin situ activity in the alkaline mesenteron. Proteinase activity, however, had an optimum at pH >12, suggesting that the digestion of bacteria in the bibionid gut is caused by a combination of digestive proteinases and alkaline pH in the anterior mesenteron.

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References

  • Anderson J.M., Bignell D.E.: Bacteria in the food, gut contents and feces of the litter feeding millipedeGlomeris marginata (Villers).Soil Biol.Biochem. 12, 251–254 (1980).

    Article  Google Scholar 

  • Anderson J.M., Ineson P.: Interaction between microorganisms and soil invertebrates in nutrient flux pathways of forest ecosystems, pp. 59–88 in J.M. Anderson, A.D. Rayner, D.W.H. Walton (Eds):Invertebrate Microbial Interactions. Cambridge University Press, Cambridge (UK) 1984.

    Google Scholar 

  • Bloem J.: Fluorescent staining of microbes for total counts, pp. 1–12 in A.D.L. Akkermans, J.D. Elsas, F.J. Bruijn (Eds):Molecular Microbial Ecology Manual. Kluwer Academic Press, Dordrecht (The Netherlands) 1995.

    Google Scholar 

  • Brune A., Kühl M.: pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes.J.Insect Physiol. 42, 1121–1127 (1996).

    Article  CAS  Google Scholar 

  • Brune A., Emerson D., Breznak J.A.: The termite 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 (1995).

    PubMed  CAS  Google Scholar 

  • Byzov B.A., Kurakov A.V., Tretyakova E.B., Thanh V.N., To Luu N.D., Rabinovich Y.M.: Principles of the digestion of microorganisms in the gut of soil millipedes: specificity and possible mechanisms.Appl.Soil Ecol. 9, 149–156 (1998).

    Article  Google Scholar 

  • Frouz J.: Use of soil dwellingDiptera (Insecta, Diptera) as bioindicators: a review of ecologigal requirements and response to disturbance.Agr.Ecosyst.Environ. 74, 167–186 (1999).

    Article  Google Scholar 

  • Frouz J., Šustr V.: The impact of drying and rewetting of leaf litter on feeding activity ofBibio pomonae (Diptera: Bibionidae) larvae.Studia Dipterol. 3, 101–106 (1996).

    Google Scholar 

  • Frouz J., Šantrůčkova H., Elhottová D.: The effect of bibionid larvae feeding on the microbial community of litter and on reconsumed excrements.Pedobiologia 43, 221–230 (1999).

    Google Scholar 

  • Frouz J., Elhottova D., Šustr V., Krištůfek V., Hubert J.: Preliminary data about compartmentalization of the gut of saprophagous diptera larvaePenthetria holosericea (Bibionidae).Eur.J.Soil Biol. 38, 47–51 (2002).

    Article  Google Scholar 

  • Gunnarson T., Tunlid A.: Recycling of fecal pellets in isopods: microorganisms and nitrogen compounds as potential food source forOniscus asellus L.Soil Biol.Biochem. 18, 595–600 (1986).

    Article  Google Scholar 

  • Hassall M., Turner J.G., Rands M.R.W.: Effect of terrestrial isopods on the decomposition of woodland leaf litter.Oecologia 72, 597–604 (1987).

    Article  Google Scholar 

  • Hopkins D.W., Chudek J.A., Bignell D.E., Frouz J., Webster E.A., Lawson T.: Application of13C NMR to investigate the transformations and biodegradation of organic materials by some soil and litter-dwelling insects.Biodegradation 9, 423–431 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Hopkins D.W., Frouz J., Šustr V., Chudek J.A.: Preliminary observation of solid state13C NMR on carbon transformation in leaf litter during feeding by two soil invertebrates, pp. 91–96 in K. Tajovský, V. Pižl (Eds):Soil Zoology in Central Europe. Institute of Soil Biology, České Budějovice (Czechia) 1999.

    Google Scholar 

  • Ji R., Brune A.: Transformation and mineralization of14C-labeled cellulose, peptidoglycan, and protein by the soil-feeding termiteCubitermes orthognatus.Biol.Fertil.Soils 33, 166–174 (2001).

    Article  CAS  Google Scholar 

  • Ji R., Kappler A., Brune A.: Transformation and mineralization of synthetic14C-labeled humic model compounds by soil-feeding termites.Soil.Biol.Biochem. 32, 1281–1291 (2000).

    Article  CAS  Google Scholar 

  • Johnson K. S., Felton G.W.: Potential influence of midgut pH and redox potential on protein utilization in insect herbivores.Arch.Insect Biochem.Physiol. 32, 85–105 (1996).

    Article  CAS  Google Scholar 

  • Ladd J.N., Butler J.H.A.: Short term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates.Soil Biol.Biochem. 4, 19–30 (1972).

    Article  CAS  Google Scholar 

  • Krištůfek K., Ravas K., Piži V.: Changes in density of bacteria and microfungi during gut transit inLumbricus rubellus andAporrectodea caliginosa (Oligochaeta: Lumbricidae).Soil Biol.Biochem. 24, 1499–1500 (1992).

    Article  Google Scholar 

  • Krištůfek V., Nováková A., Pižl V.: Coprophilous streptomycetes and fungi — food sources for enchytraeid worms (Enchytraeidae).Folia Microbiol. 46, 555–558 (2001).

    Article  Google Scholar 

  • Nováková A., Frouz J.: The effect of feeding of bibionid larvae on composition of litter microfungal community, pp. 233–248 in K. Tajovský, V. Pižl (Eds):Soil Zoology in Central Europe. Institute of Soil Biology, České Budějovice (Czechia) 1999.

    Google Scholar 

  • Pobozsny M.: On the feeding biology of larval St. Mark’s flyBibio marci L. (Diptera: Bibionidae).Acta Zool.Acad.Sci.Hung. 27, 355–360 (1982).

    Google Scholar 

  • Reyes V.G., Tiedje J.M.: Ecology of the gut microflora ofTracheoniscus rathkei.Pedobiologia 16, 67–74 (1976).

    Google Scholar 

  • Scheu S., Wolters V.: Influence of fragmentation and bioturbation on the decomposition of14C-labelled beach litter.Soil Biol.Biochem. 23, 1029–1034 (1991).

    Article  CAS  Google Scholar 

  • Šustr V., Frouz J.: Activity of carbohydrases in the gut ofBibionidae larvae (Diptera).Eur.J.Soil Biol. 38, 75–77 (2002).

    Article  Google Scholar 

  • Szabó I.M.:Microbial Communities in Forest Rendzina Ecosystem, pp. 1–415. Akademia Kiadó, Budapest 1974.

    Google Scholar 

  • Szlavecz K., Pobozsny M.: Coprophagy in isopods: cause for indirect interaction.Ann.Zool.Fenici 196, 124–128 (1995).

    Google Scholar 

  • Taylor C.B.: The nutritional requirements of the predominant bacterial flora of the soil.Proc.Soc.Appl.Bacteriol. 14, 101–111 (1951).

    Google Scholar 

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Correspondence to J. Frouz.

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This study was supported by grant B606 6903 of theGrant Agency of Academy of Sciences of the Czech Republic and grant MSM 123 100 004 of theMinistry of Education, Youth and Sports of the Czech Republic.

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Frouz, J., Krištůfek, V., Li, X. et al. Changes in amount of bacteria during gut passage of leaf litter and during coprophagy in three species ofBibionidae (Diptera) larvae. Folia Microbiol 48, 535–542 (2003). https://doi.org/10.1007/BF02931337

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  • DOI: https://doi.org/10.1007/BF02931337

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