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Mutualism and biodiversity in soils

  • Biodiversity And Ecosystem Process
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Abstract

Most soil invertebrates and roots have developed strong interactions with micro-organisms to exploit the organic and mineral resources of soil. Micro-fauna are mainly predators of microorganisms whereas larger organisms interact with micro-organisms through the “external rumen” or facultative endosymbiotic digestive systems. Mobilisation of nutrient and organic resources through mutualism with soil microflora seems to be all the more efficient as the organisms are large (like e.g., roots, termites or earthworms) and temperature is high. In the humid tropics, part of the existing species richness may have originated from an increased base of resources resulting from the development of mutualistic relationships. Evidence for this process is given for earthworm communities. Consequences for soil function and the species richness of plants and consumers are discussed.

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References

  • Abbadie L and Lepage M 1989 The role of subterranean fungus comb chambers (Isoptera, Macrotermitine) in soil nitrogen cycling in a preforest savanna (Côte d'Ivoire). Soil Biol. Biochem. 21 (8), 1067–1071.

    Google Scholar 

  • Bachman G and Kinzel H 1992 Biochemical screening of the soilroot system of six different plants. Soil Biol. Biochem. 24, 543–552.

    Google Scholar 

  • Barois I 1987 Interactions entre les Vers de Terre (Oligochaeta) tropicaux géophages et la microflore pour l'exploitation de la matière organique du sol. Thèse Université Paris VI.

  • Barois I and Lavelle P 1986 Changes in respiration rate and some physicochemical properties of a tropical soil during transit throughPontoscolex corethrurus (Glossoscolecidae, Oligochaeta). Soil Biol. Biochem. 18, 539–541.

    Google Scholar 

  • Barois I 1992 Mucus production and microbial activity in the gut of two species ofAmynthas from cold and warm tropical climates. Soil Biol. Biochem. 24, 1507–1510.

    Google Scholar 

  • Barois I, Verdier B, Kaiser P, Mariotti A, Rangel P and Lavelle P 1987 Influence of the tropical earthwormPontoscolex corethrurus (Glossoscolecidae) on the fixation and mineralization of nitrogen. pp 151–158.In On Earthworms. Eds. P Omodeo and A M Bonvicini. Mucchi, Bologna, Italy.

    Google Scholar 

  • Begon M, Harper J L and Townsend C R 1990 Ecology, Individuals, Populations and communities. Second edition. Blackwell Scientific Publications, Boston, Oxford, London.

    Google Scholar 

  • Billes G, Gandais-Riollet N and Bottner P 1986 Effets d'une culture de graminées sur la décomposition d'une litière végetale marquée au14C et15N dans le sol en conditions contrôlées. Oecol. Plant. 7, 273.

    Google Scholar 

  • Boettcher S E and Kalisz P J 1992 Single-tree influence on soil properties in the mountains of eastern Kentucky. Ecology 71, 1365–1372.

    Google Scholar 

  • Boettcher S E and Kalisz P J 1991 Single-tree influence on earthworms in forest soils in eastern Kentucky. Soil Sci. Soc. Am. J. 55, 862–865.

    Google Scholar 

  • Bouché M B 1977 Stratégies lombriciennes. Soil Organisms as Components of Ecosystems. Ecol. Bull. (Stockholm) 25, 122–132.

    Google Scholar 

  • Bowen G and Theodorou C 1973 Growth of ectomycorrhizal fungi around seeds and roots.In Ectomycorrhizae: their Ecology and Physiology. Eds. G C Marks and T Kozlowski. pp 119–126. Academic Press, New York.

    Google Scholar 

  • Breland T A and R B L 1991 Microbial growth and nitrogen immobilization in the root zone of barley (Hordeum vulgare L.), Italian ryegrass (Lolium multiflorum Lam.), and white clover (Trifolium repens L.) Biol. Fert. Soils 12, 154–160.

    Google Scholar 

  • Breznak J A 1984 Biochemical aspects of symbiosis between termites and their intestinal microbiota. pp 173–204.In Invertebrate-microbial Interactions. Eds. J M Anderson, A D M Rayner and D W H Walton. Cambridge University Press, Cambridge.

    Google Scholar 

  • Brusewitz G 1959 Untersuchungen über den Einfluss des Regenwurms auf Zahl, Art und Leistungen von Mikroorganismen in Boden. Arch. Mikrobiol. 33, 52–82.

    Google Scholar 

  • Campbell W G 1929 The chemical aspect of the destruction of oakwood by powderpost and death-watch beetles,Lyctus spp andXestobium sp. Biochem. J. 23, 1290–1293.

    Google Scholar 

  • Chaussod R, Houot S, Guiraud G and Hétier J M 1988 Size and turnover of the microbial biomass in agricultural soils: laboratory and field measurements.In Nitrogen efficiency in agricultural soils. Eds. K A Smith and D S Jenkinson. pp 321–326. Applied Sciences, Elsevier, London.

    Google Scholar 

  • Clarholm M and Rosswall T 1980 Biomass and turnover of bacteria in a forest soil and a peat. Soil Biol. Biochem. 12, 49–57.

    Google Scholar 

  • Clarholm M 1985 Interactions of bacteria, protozoa and plant leading to mineralization of soil nitrogen. Soil Biol. Biochem. 17, 181–187.

    Google Scholar 

  • Coleman D C, Ingham R E, McClellan J F and Trofymow J A 1984 Soil nutrient transformations in the rhizosphere via animalmicrobial interactions.In Invertebrates-Microbial Interactions. Eds. J M Anderson, A D M Rayner and D W H Walton. pp 35–58. Cambridge University Press, Cambridge.

    Google Scholar 

  • Curl E A and Truelove B 1986 The Rhizosphere. Springer-Verlag, Berlin. 288p.

    Google Scholar 

  • Daniel O and Anderson J M 1992 Microbial biomass and activity in contrasting soil materials after passage through the gut of the earthwormLumbricus rubellus Hoffmeister. Soil Biol. Biochem. 24 (5), 465–470.

    Google Scholar 

  • Darbyshire J F and Greaves M P 1967 Protozoa and bacteria in the rhizosphere ofSinapis alba L.,Trifolium repens L., andLolium perenne L. Can. J. Microbiol. 13, 1057–1068.

    Google Scholar 

  • Darlington J P E C 1982 The underground passages and storage pits used in foraging by a nest of the termiteMacrotermes michaelseni in Kajiado, Kenya. Ken. J. Zool. 198, 237–247.

    Google Scholar 

  • Devigne J and Jeuniaux C 1961 Origine tissulaire des enzymes chitinolytiques intestinaux des lombrics. Arch. Int. Physiol. Biochim. 69, 223–234.

    Google Scholar 

  • Dowding P 1976 Allocation of resources, nutrient uptake and release by decomposer organisms.In The Role of Terrestrial and Aquatic Organisms in Decomposition Processes. The 17th Symposium of the British Ecological Society. Eds. J M Anderson and A Macfadyen. pp 169–183. Blackwell Scientific Publications, Oxford, Great Britain.

    Google Scholar 

  • Fitter A H 1985 Functional significance of root morphology and root system architecture.In Ecological Interactions in Soil, Plants, Microbes and Animals, Eds. D Atkinson, A H Fitter D I Read and M B Usher. pp 87–106 Blackwell Scientific Publications, Oxford, Great Britain.

    Google Scholar 

  • Fogel R 1985 Roots as primary producers in below-ground ecosystems.In Ecologiacal Interactions in Soil, Plant, Microbes and Animals. Eds. D Atkinson, A H Fitter D J Read and M B Usher. pp 23–36, Blackwell Scientific Publications, Oxford, Great Britain.

    Google Scholar 

  • Foster R C and Rovira A D 1978 The ultrastructure of the rhizosphere ofTrifolium subterraneum L.In Microbial Ecology. Eds. M W Loutit and J A R Miles. pp 278–290. Springer Verlag, Berlin Heildelberg.

    Google Scholar 

  • Garnier-Sillam E, Toutain F, Villemin G and Renoux J 1988 Transformation de la matière organique végétale sous l'action du termiteMacrotermes mülleri (Sjöstedt) et de son champignon symbiotique. Can. J. Microbiol. 34, 1247–1255.

    Google Scholar 

  • Garnier-Sillam E and Renoux J 1989 Les composés humiques des termitières deThoracotermes macrothorax (humivore) et deMacrotermes mülleri (champignonniste). Soil Biol. Biochem. 21, 499–505.

    Google Scholar 

  • Gilot C, Lavelle P, Kouassi Ph and Guillaume G 1994 Biological activity of soils.In Hevea Stands of Different Ages in Côte d'Ivoire. Zool. Fenn. (In press).

  • Gourbière F 1982 Pourriture blanche de la litière d'Abies alba Mill. I. — Evolution de la litière sous l'action des Basidiomycètes du genreCollybia. Rev. Ecol. Biol. Sol 19, 163–175.

    Google Scholar 

  • Gourbière F 1983 Pourriture blanche de la litière d'Abies alba Mill. II. — Répartition spatio-temporelle et activité annuelle des Basidiomycètes de genreCollybia. Rev. Ecol. Biol. Sol 20, 461–474.

    Google Scholar 

  • Grassé P P 1984 Termitologia, Masson, Paris.

    Google Scholar 

  • Hassal M and Rushton S P 1982 The role of coprophagy in the feeding strategies of terrestrial isopods. Oecologia 53, 374–381.

    Google Scholar 

  • Howe H F 1984 Constraints on the evolution of mutualisms. Am. Nat. 123, 764–772.

    Google Scholar 

  • Janzen D H 1985 Natural history of mutualism.In Biology of Mutualism. Ecology and Evolution. Ed. D H Boucher. pp 40–99. Croom. Helm, London, Sydney.

    Google Scholar 

  • Jenkinson D S 1966 The Priming Action. J. Appl. Radiat. Isotopes, Suppl. XX, 199–208.

  • Jenkinson D S and Ladd J N 1981 Microbial biomass in soil: measurement and turnover.In Soil Biochemistry. Eds. J N Ladd and E A Paul. pp 415–417. New York.

  • Jones D L and Darrah P R 1992 Re-sorption of organic components by roots ofZea mays L. and its consequences in the rhizosphere; I. Re-sorption of14C labelled glucose, mannose and citric acid. Plant and Soil 143, 259–266.

    Google Scholar 

  • Kirk T K and Farrell R L 1987 Enzymatic “combustion”: the microbial degradation of lignin. Ann. Rev. Microbiol. 41, 465–505.

    Google Scholar 

  • Kretzschmar A 1982 Description des galeries de vers de terre et variations saisonnières des réseaux (observations en conditions naturelles). Rev. Ecol. Biol. Sol 19, 579–591.

    Google Scholar 

  • Lavelle P 1978 Les Vers de Terre de la savane de Lamto (Côte d'Ivoire): peuplements, populations et fonctions dans l'écosystème. Thèse d'Etat, Paris VI. Publication du Laboratoire de Zoologie de I'ENS 12.

  • Lavelle P 1981 Stratégies de reproduction chez les vers de terre. Acta Oecol. (Oecol. gener.) 2, 117–133.

    Google Scholar 

  • Lavelle P 1983 The structure of earthworm communities.In Earthworm Ecology: from Darwin to Vermiculture. Ed. J E Satchell. pp 449–466. Chapman and Hall, London.

    Google Scholar 

  • Lavelle P, Zaidi Z and Schaefer R 1983 Interactions between earthworms, soil organic matter and microflora in an African savanna soil.In New Trends in Soil Biology. Eds. Ph Lebrun, A M André, Ade Medts, C Gregoire-Wibo and G Wauthy. pp 253–259. Dieu-Brichard, Louvain-la-Neuve.

    Google Scholar 

  • Lavelle P 1986 Associations mutualistes avec la microflore du sol et richesse spécifique sous les tropiques: l'hypothése du premier maillon. C.R. Acad. Sci. Paris 302, 11–14.

    Google Scholar 

  • Lavelle P, Rangel P and Kanyonyo J 1983 Intestinal mucus production by two species of tropical earthworm:Millsonia lamtoiana (Megascolecidae) andPontoscolex corethrurus (Glossoscolecidae).In New Trends in Soil Biology. Eds. Ph Lebrun, A M André, Ade Medts, C Gregoire-Wibo, and G Wauthy. pp 405–410. Dieu-Brichard, Louvain-la-Neuve.

    Google Scholar 

  • Lavelle P and Martin A 1992 Small-scale and large-scale effects of endogeic earthworms on soil organic matter dynamics in soils of the humid tropics. Soil Biol. Biochem. 24, 1491–1498.

    Google Scholar 

  • Lavelle P, Blanchart E, Martin A, Martin S, Toutain F, Barois I and Schaefer 1994 A hierarchical model for decomposition in terrestrial ecosystems: Application to soils of the humid tropics. Biotropica 25, 130–150.

    Google Scholar 

  • Lavelle P and Gilot C 1994 Priming effects of macroorganisms on microflora: a key process of soil function?In Beyond the Biomass. Eds. K Ritz, J Dighton and K Giller, p 6. Wiley-Sayce, UK.

    Google Scholar 

  • Laverack M S 1963 The Physiology of Earthworms. Pergamon Press, Oxford.

    Google Scholar 

  • Lee K E and Wood T G 1971 Termites and Soils. Academic Press, London.

    Google Scholar 

  • Lee K 1985 Earthworms: Their Ecology and Relationships with Soils and Land Use. Academic Press, New York.

    Google Scholar 

  • Lepage M 1983 Structure et dynamique des peuplements de termites tropicaux. Acta Oecol./Oecol. Gener. 4, 65–87.

    Google Scholar 

  • Leroy C, Toutain F and Lavelle P 1993 Variations des caractéristiques de l'humus forestier d'un sol ferrallitique (Guyane) selon l'essence arborée considérée. Résultats préliminaires. Cah. Pedo. ORSTOM (In press).

  • Lespinat P A and Berlier Y 1975 Les facteurs externes agissant sur l'excrétion racinaire. Soc. Bot. Fr., Coll. Rhizospère XX, 21–30.

  • Levieux J 1976 Deux aspects de l'action des fourmis (Hymenoptera, Formicidae) sur le sol d'une savane préforestière de Côte d'Ivoire. Bull. Ecol. 7, 283–295.

    Google Scholar 

  • Lewis D H 1985 Symbiosis and mutualism: crisp concepts and soggy semantics.In Biology of Mutualism. Ed. D H Boucher. pp 29–43. Croom Helm, Beckenham.

    Google Scholar 

  • Li D-M and Alexandrer M 1986 Bacterial growth rates and competition affect nodulation and root colonization byRhizobium meliloti Appl. Env. Microbiol. 52, 807–811.

    Google Scholar 

  • Loquet M and Vinceslas M 1987 Cellulolyse et lignilolyse liées au tube digestif d'Eisenia foetida andrei Bouché. Rev. Ecol. Biol. Sol. 24, 559–571.

    Google Scholar 

  • Margulis L 1981 Symbiosis in Cell Evolution: Life and its Environment on the Early Earth. W H Freeman, San Francisco, CA.

    Google Scholar 

  • Martens R 1990 Contribution of rhizodeposits to the maintenance and growth of soil microbial biomass. Soil Biol. Biochem. 22, 141–147.

    Google Scholar 

  • Martin A 1989 Effets des Vers de Terre tropicaux géophages sur la dynamique de la matière organique du sol dans les savanes tropicales humides. Thése de l'Université, Paris XI.

  • Martin A 1991 Short-term and long-term effect of the endogeic earthwormMillsonia anomala (Omodeo) (Megascolecidae, Oligochaeta) of a tropical savanna, on soil organic matter. Biol. Fert. Soil 11, 234–238.

    Google Scholar 

  • Martin A, Cortez J, Barois I and Lavelle P 1987 Les mucus intestinaux de ver de terre, moteur de leurs interactions avec la microflore. Rev. Ecol. Biol. Sol 24, 549–558.

    Google Scholar 

  • Martin A, Mariotti A, Balesdent J and Lavelle P 1991 Soil organic matter assimilation of a geophagous tropical earthworm based on 13C measurements. Ecology 73, 118–128.

    Google Scholar 

  • Martin A, Balesdent J and Mariotti A 1992 Earthworm diet related to soil organic matter dynamics through 13C measurements. Oecologia 91, 23–29.

    Google Scholar 

  • Martin M M 1984 The role of digested enzymes in digestive processes of insects.In Invertebrates — Microbial Interactions. Eds. J M Anderson, A D M Rayner and D W H Walton. pp 155–172. Cambridge University Press, Cambridge.

    Google Scholar 

  • Meyer J A 1960 Résultats agronomiques d'un essai de nivellement des termitières réalisé dans la cuvette centrale Congolaise. Bull. Agric. Congo Belge 51, 1047–1059.

    Google Scholar 

  • Mills J T and Sinha R N 1971 Interactions between a springtail,Hypogastrura tullbergi, and soil-borne fungi. J. Econ. Entomol. 64, 398–401.

    Google Scholar 

  • Moore J C 1988 The influence of Microarthropods on symbiotic and non-symbiotic mutualism in detrital-based below-ground foodwebs. Agric. Ecos. Environ. 24, 147–159.

    Google Scholar 

  • Newman E I 1985 The rhizosphere: carbon sources and microbial populations.In Ecological Interactions in Soil, Plants, Microbes and Animals. Eds. D Atkinson, A H Fitter, D J Read and M B Usher. pp 107–121. Blackwell Scientific Publications, Oxford, Great Britain.

    Google Scholar 

  • Parle J N 1963 Micro-organisms in the intestines of earthworms. J. Gen. Microbiol. 31, 1–11.

    Google Scholar 

  • Parmelee R W, Ehrenfeld J G and Tate R L 1993 Effects of pine roots on microorganisms, fauna, and nitrogen availability in two soil horizons of a coniferous forest spodosol. Biol. Fert. Soils 15, 113–119.

    Google Scholar 

  • Ponge J F and Carpentier M J 1981 Etude des relations microflore-microfaune: expériences surPseudosiniella alba (Packard), Collembole mycophage. Rev. Ecol. Biol. Sol 18, 291–303.

    Google Scholar 

  • Potts R C and Hewitt P H 1974 Some properties and reaction characteristics of the partially purified cellulase from the termiteTrinervitermes trinervoides (Nasutitermitidae). Comp. Biochem. Physiol. 47B, 327–337.

    Google Scholar 

  • Rouland C, Civas A, Renoux J and Petek F 1988 Synergistic activities of the enzymes involved in cellullose degradation, purified fromMacrotermes mölleri and from its symbiotic fungusTermitomyces sp. 91 B (3), 459–465.

  • Rouland C, Bra Keleke S, Labat M, Mora P and Renoux J 1990 Endosymbiosis and exosymbiosis in the fungus-growing termites.In Microbiology in Poecilotherms. Ed. R Lésel. pp 79–82. Elsevier Biomedical Division, Amsterdam.

    Google Scholar 

  • Scheu S 1987 Microbial activity and nutrient dynamics in earthworm casts (Lumbricidae). Biol. Fert. Soils 5, 230–234.

    Google Scholar 

  • Shaw C and Pawluk S 1986 Faecal microbiology ofOctolasium tyrtaeum, Apporectodea turgida andLumbricus terrestris and its relation to the carbon budgets of three artificial soils. Pedobiologia 29, 377–389.

    Google Scholar 

  • Spain A V, Safigna P G and Wood A W 1990 Tissue carbon sources forPontoscolex corethrurus (Oligochaeta, Glossoscolecidae) in a sugarcane ecosystem. Soil. Biol. Biochem 22, 703–706.

    Google Scholar 

  • Swift M J, Heal O W and M A J 1979 Decomposition in Terrestrial Ecosystems. Blackwell Scientific Publ., Oxford.

    Google Scholar 

  • Topp E, Scheunert I, Attar A and Korte F 198 Factors affecting the uptake of14C-labeled organic chemicals by plants from soil. Ecotoxicol. Environ. Safe 11, 219–228.

  • Toutain F 1987 Les litières: sièges de systèmes interactifs et moteurs de ces interactions. Rev. Ecol. Biol. Sol 24, 231–242.

    Google Scholar 

  • Trigo D and Lavelle P 1992 Changes in respiration rate and some physico-chemical properties of soil during gut transit throughAllolobophora molleri (Lumbricidae). Biol. Fert. Soil 15, 185–188.

    Google Scholar 

  • Trigo D, Martin A and Lavelle P 1992 A mutualist system of digestion in temperate earthwormsAllolobophora molleri andOctolasium lacteum. (Lumbricidae). Zool. Fenn. (In press).

  • Trofymow J A and Coleman D C 1982 The role of bacterivorous and fungivorous nematodes in cellulose and chitin decomposition.In Nematodes in Soil Ecosystems. Ed. D W Freckman. pp 117–138. University of Texas Press, Austin.

    Google Scholar 

  • Urbasek F 1990 Cellulase activity in the gut of some earthworms. Rev. Ecol. Biol. Sol 27, 21–28.

    Google Scholar 

  • Urbasek F and Chalupsky JJr 1991 Activity of digestive enzymes in 4 species of Enchytraeidae (Oligochaeta). Rev. Ecol. Biol. Sol 28, 145–154.

    Google Scholar 

  • Urbasek F and Pizl V 1991 Activity of digestive enzymes in the gut of five earthworm species (Oligochaeta, Lumbricidae). Rev. Ecol. Biol. Sol 28, 461–468.

    Google Scholar 

  • Vannier G 1979 Relations trophiques entre la microfaune et la microflore du sol; aspects qualitatifs et quantitatifs. Boll. Zool. 46, 343–361.

    Google Scholar 

  • Vannier G 1985 Modes d'exploitation et partage des ressources alimentaires dans le système saprophage par les microarthropodes du sol. Bull. Ecol. 16, 19–34.

    Google Scholar 

  • Wood T G 1988 Termites and soil environment. Biol. Fert. Soils 6, 228–236.

    Google Scholar 

  • Yamin M A 1981 Cellulose metabolism by the flagellateTrichonympha from a termite is independent of endosymbiotic bacteria. Science 211, 58–59.

    Google Scholar 

  • Youssef R A, Kanazawa S and Chino M 1989 Distribution of microbial biomass across the rhizosphere of barley (Hordeum vulgare L.) in soils. Biol. Fert. Soils 7, 341–345.

    Google Scholar 

  • Zhang B G, Rouland C, Lattaud C and Lavelle P 1993 Origin and activity of enzymes found in the gut content of the tropical earthwormPontoscolex corethrurus Müller. Eur. J. Soil Biol. 29, 7–11.

    Google Scholar 

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Authors and Affiliations

  1. Laboratoire d'Ecologie des Sols Tropicaux, Orstom, 72 route d'Aulnay, 93143, Bondy Cedex, France

    P. Lavelle & C. Lattaud

  2. Departamento Biologia Animal 1, Universidad Complutense, 28040, Madrid, Spain

    D. Trigo

  3. Instituto de Ecologia, AP 63, 91000, Xalapa, Ver, Mexico

    I. Barois

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  1. P. Lavelle
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Lavelle, P., Lattaud, C., Trigo, D. et al. Mutualism and biodiversity in soils. Plant Soil 170, 23–33 (1995). https://doi.org/10.1007/BF02183052

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