Abstract
Although microorganisms are largely responsible for organic matter decomposition, earthworms may also affect the rates of decomposition directly by feeding on and digesting organic matter and microorganisms, or indirectly affect them through their interactions with the microorganisms, basically involving stimulation or depression of the microbial populations. We tested the general hypothesis that microbial populations, and especially fungi, are enhanced by earthworm activity, and also whether earthworms are able to modify the biodiversity of microbial populations, and its relation to the function of the system. In addition, we examined the metabolic quotient and the effect of labile organic C to assess the relationships between earthworm and microbes. We found that decomposition of pig manure has two stages characterized by the presence or absence of earthworms. Thus, the presence of earthworms was related with increases in overall microbial biomass and activity, which decreased when earthworms left the substrate; the same pattern was observed for fungi. Furthermore, earthworms modified the physiological profiles of microbial communities of pig manure, increasing the diversity of substrates utilized. In addition, earthworms promoted a more efficient use of energy of microbial communities, as the metabolic quotient showed. The rate of carbon loss was almost twice where earthworms were present, revealing faster decomposition. Our data match with the recent findings that to maintain essential processes the functional properties of present species are at least as important as the number of species per se. This is in accordance with the “insurance hypothesis,” which states that a large number of species is probably essential for maintaining stable processes in changing environments, as the presence of earthworms would have promoted in pig manure.
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References
Aira, M, Monroy, F, Domínguez, J (2006) Eisenia fetida (Oligochaeta, Lumbricidae) activates fungal growth, triggering cellulose decomposition during vermicomposting. Microb Ecol (in press, doi:10.1007/s00248-006-9109-x)
Aira, M, Monroy, F, Domínguez, J (2005) Ageing effects on nitrogen dynamics and enzyme activities in casts of Aporrectodea caliginosa (Lumbricidae). Pedobiologia 49: 467–473
Anderson, JPE (1982) Soil respiration. In: Page AL (Ed.) Methods of soil analysis, Part 2. Chemical and microbiological properties. American Society of Agronomy, Madison, Wisconsin, pp 831–871
Anderson, JPE, Domsch, KH (1993) The metabolic quotient for CO2 (qCO2) as a specific activity parameter to assess the effects of environmental conditions, such as pH, on the microbial biomass of forest soils. Soil Biol Biochem 25: 393–395
Andren, O, Balandreau, J (1999) Biodiversity and soil functioning— from black box to can of worms? Appl Soil Ecol 13: 105–108
Bardgett, RD, Shine A (1999) Linkages between plant litter diversity, soil microbial biomass and ecosystem function in temperate grasslands. Soil Biol Biochem 31: 317–321
Bossio, DA, Scow, KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35: 265–278
Brown, GG, Barois, I, Lavelle, P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 36: 177–198
Dash, HK, Beura, BN, Dash, MC (1986) Gut load, transit time, gut microflora, and turnover of soil, plant, and fungal material by some tropical earthworms. Pedobiologia 29: 13–20
Devliegher, W, Verstraete, W (1995) Lumbricus terrestris in a soil core experiment—nutrient-enrichment processes (NEP) and gut-associated processes (GAP) and their effect on microbial biomass and microbial activity. Soil Biol Biochem 27: 1573–1580
Domínguez, J (2004) State of the art and new perspectives on vermicomposting research. In: Edwards CA (Ed.) Earthworm ecology, 2nd edition, CRC Press, Boca Raton, pp 401–424
Doube, BM, Brown, GG (1998) Life in a complex community: functional interactions between earthworms, organic matter, microorganisms, and plant growth. In: Edwards CA (Ed.) Earthworm ecology, St. Lucie Press, Boca Raton, pp 179–211
Edwards, CA (1998) Earthworm Ecology. St. Lucie Press, Boca Raton
Egert, M, Marhan, S, Wagner, B, Scheu, S, Friedrich, MW (2004) Molecular profiling of 16S rRNA genes revealed diet-related differences of microbial communities in soil, gut and casts of Lumbricus terrestris L. (Oligochaeta: Lumbricidae). FEMS Microbiol Ecol 48: 187–197
Garland, JL (1997) Analysis and interpretation of community-level physiological profiles in microbial ecology. FEMS Microbiol Ecol 24: 289–300
Garrett, SD (1981) Soil fungi and soil fertility. Pergamon Press, Oxford
Griffiths, BS, Bonkowski, M, Roy, J, Ritz K (2001) Functional stability, substrate utilization and biological indicators of soils following environmental impacts. Appl Soil Ecol 16: 49–61
Hill, GT, Mitkowski, NA, Aldrich-Wolfe, L, Emele, LR, Jurkonie, DD, Ficke A, Maldonado-Ramirez S, Lynch ST, Nelson EB (2000) Methods for assessing the composition and diversity of soil microbial communities. Appl Soil Ecol 15: 25–36
Ibekwe, AM, Kennedy, AC (1998) Phospholipid fatty acid profiles and carbon utilization patterns for analysis of microbial community structure under field and greenhouse conditions. FEMS Microbiol Ecol 26: 151–163
Jackson, ML (1958) Soil chemical analysis. Constable & Co. Ltd, London
Jones, CG, Lawton, JH, Shachak, M (1994) Organisms as ecosystem engineers. Oikos 69: 373–386
Lavelle, P, Bignell, D, Lepage, M, Wolters, V, Roger, P, Ineson, P, Heal, OW, Ghillion, S (1997) Soil function in a changing world: The role of invertebrate ecosystem engineers. Eur J Soil Biol 33: 159–193
Lavelle, P, Spain, AV (2001) Soil ecology. Kluwer Academic Press, London
Logan, NA (1994) Bacterial systematics. Blackwell Scientific, London
Loquet, M, Bhatnagar, T, Bouché, MB, Rouelle, J (1977) Essai d’estimation de l’influence écologique des lombriciens sur les microorganismes. Pedobiologia 17: 400–417
Loreau, M, Naeem, S, Inchausti, P, Bengtsson, J, Grime, JP, Hector, A, Hooper, DU, Huston, MA, Raffaelli, D, Schmid, B, Tilman, D, Wardle, DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294: 804–808
McLean, MA, Parkinson, D (1998) Impacts of the epigeic earthworm Dendrobaena octaedra on microfungal community structure in pine forest floor: a mesocosm study. Appl Soil Ecol 8: 61–75
McLean, MA, Parkinson, D (2000) Field evidence of the effects of the epigeic earthworm Dendrobaena octaedra on the microfungal community in pine forest floor. Soil Biol Biochem 32: 351–360
Moody, SA, Briones, MJI, Pierce, TG, Dighton, J (1995) Selective consumption of decomposing wheat straw by earthworms. Soil Biol Biochem 28: 533–537
Saetre, S (1998) Decomposition, microbial community structure, and earthworm effects along a birch–spruce soil gradient. Ecology 79: 834–846
Scheu S (1987) Microbial activity and nutrient dynamics in earthworm cast (Lumbricidae). Biol Fertil Soils 5: 230–234
Scheu S, Schaefer M (1998) Bottom-up control of the soil macrofauna community in a beechwood on limestone: manipulation of food resources. Ecology 79: 1573–1585
Scheu, S, Schlitt, N, Tiunov, AV, Newington, JE, Jones, TF (2002) Effects of the presence and community composition of earthworms on microbial community functioning. Oecologia 133: 254–260
Schönholzer, F, Hahn, D, Zeyer, J (1999) Origins and fate of fungi and bacteria in the gut of Lumbricus terrestris L. studied by image analysis. FEMS Microbiol Ecol 28: 235–248
Scott, JS, Knudsen, GR (1999) Soil amendment effects of rape (Brassica napus) residues on pea rhizosphere bacteria. Soil Biol Biochem 31: 1435–1441
Siciliano, SD, Germida, JJ (1998) Biolog analysis and fatty acid methyl esther profiles indicate that pseudomonad inoculants that promote phytoremediation alter the root-associated microbial community of Bromus biebersteinii. Soil Biol Biochem 30: 1717–1723
Smalla, K, Wachtendorf, U, Heuer, H, Liu, WT, Forney L (1998) Analysis of Biolog BG substrate utilization patterns by microbiological communities. Appl Environ Microbiol 64: 1220–1225
Tiunov, AV, Dobrovolskaya, TG, Polyanskaya, LM (1997) Microbial community of Lumbricus terrestris burrow walls. Microbiology 66: 349–353
Tiunov, AV, Scheu, S (1999) Microbial respiration, biomass, biovolume and nutrient status in burrow walls of Lumbricus terrestris L. (Lumbricidae). Soil Biol Biochem 31: 2039–2048
Tiunov, AV, Scheu, S (2000) Microfungal communities in soil, litter and cast of Lumbricus terrestris L. (Lumbricidae): a laboratory experiment. Appl Soil Ecol 14: 17–26
Tiunov, AV, Scheu, S (2004) Carbon availability controls the growth of detritivores (Lumbricidae) and their effect on nitrogen mineralization. Oecologia 138: 83–90
Tyurin, IV (1931) A new modification of the volumetric method of determining soil organic matter by means of chromic acid. Pochvovedenie 26: 36–47
Vance, ED, Brookes, PC, Jenkinson, DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19: 703–707
Visser, S (1985) Role of soil invertebrates in determining the composition of soil microbial communities. In: Fitter AH, Atkinson D, Read DJ, Usher MB (Eds.) Ecological interactions in soil, Blackwell, Oxford, pp. 297–317
von Ende, CN (2001) Repeated-measures analysis. In: Scheiner SM, Gurevitch J (Eds.) Design and analysis of ecological experiments, Oxford University Press, Oxford, pp 134–157
Whitehead, TR, Cotta, MA (2001) Characterisation and comparison of microbial populations in swine faeces and manure storage pits by 16S rDNA gene sequence analyses. Anaerobe 7: 181–187
Young, JC (1995) Microwave-assisted extraction of the fungal metabolite ergosterol and total fatty acids. J Agric Food Chem 43: 2904–2910
Zak, JC, Willig, MR, Mooread, DL, Wildman, HG (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26: 1101–1108
Zhu, J (2000) A review of microbiology in swine manure odor control. Agr Ecosyst Environ 78: 93–106
Acknowledgments
This research was supported by CICYT (AGL2003-01570) and Xunta de Galicia (PGIDIT03PXIB30102PR) grants. Manuel Aira was financially supported by a postdoctoral fellowship from Xunta de Galicia. Manuel Aira also acknowledges Paul Fraiz for his highly valuable help in language editing.
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Aira, M., Monroy, F. & Domínguez, J. Eisenia fetida (Oligochaeta: Lumbricidae) Modifies the Structure and Physiological Capabilities of Microbial Communities Improving Carbon Mineralization During Vermicomposting of Pig Manure. Microb Ecol 54, 662–671 (2007). https://doi.org/10.1007/s00248-007-9223-4
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DOI: https://doi.org/10.1007/s00248-007-9223-4