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RESEARCH ARTICLE

Aerobic microbial activity in four tropical earthworm-soil systems. A mesocosm experiment

J. Sierra A D , G. Loranger-Merciris A B , L. Desfontaines A and M. Boval C
+ Author Affiliations
- Author Affiliations

A INRA, UR1321, ASTRO Agrosystèmes Tropicaux, F-97170, Petit-Bourg, Guadeloupe, France.

B Université des Antilles et de la Guyane, UFR Sciences Exactes et Naturelles, Campus de Fouillole, F-97157, Pointe-à-Pitre, Guadeloupe, France.

C INRA, UR143, URZ Unité de Recherches Zootechniques, F-97170, Petit Bourg, Guadeloupe, France.

D Corresponding author. Email: jorge.sierra@antilles.inra.fr

Soil Research 52(6) 584-592 https://doi.org/10.1071/SR14034
Submitted: 6 February 2014  Accepted: 4 April 2014   Published: 8 August 2014

Abstract

Soil organic matter (SOM) quality and carbon (C) availability may be major features influencing the effect of earthworms on the aerobic processes in clayey tropical soils. In this study, we assessed the effect of an anecic (Polypheretima elongata), an endogeic (Pontoscolex corethrurus) and an epigeic (Eudrilus eugeniae) earthworm on the aerobic microbial activity of two tropical soils, a calcic Vertisol and an acid Ferralsol, with clay content >70% and very different organic C content and SOM stability. The soil–earthworm interaction was studied in a 6-month mesocosm experiment in a greenhouse using soils with and without (control soil) earthworm addition. Potential C mineralisation, actual net nitrogen (N) mineralisation and dehydrogenase activity (DHA), as indicators of the aerobic activity of the soils, and phosphorus (P) availability were determined during the trial. DHA was used as an indicator of the global aerobic activity. Earthworms had little effect on potential C mineralisation but significantly increased actual net N mineralisation. The increase in N mineralisation in the Vertisol was twice as great as, and longer (6 v. 3 months) than for the Ferralsol. Differences between soils for N mineralisation were associated with a less recalcitrant SOM in the Vertisol. Available P increased 10% in the earthworm treatments. Earthworm activity improved N and P availability. DHA was 15 times higher for the Vertisol than for the Ferralsol, but the positive effect of earthworms on DHA was greater for the Ferralsol. This effect was greater for E. eugeniae, probably because of surface burrows generated by this epigeic earthworm, which favoured oxygen entry into the soil. Differences between the two soils were greater for DHA than for C and N mineralisation, and this was observed for the control soils as well as for the earthworm treatments. This indicates that earthworm activity modified the rate of the aerobic processes but it did not affect the intrinsic biological properties of these tropical soils, which were controlled mainly by SOM quality and C availability.

Additional keywords: Eudrilus eugeniae, Ferralsol, Polypheretima elongata, Pontoscolex corethrurus, SOM mineralisation, Vertisol.


References

Barot S, Ugolini A, Bekkal Brikci F (2007) Nutrient cycling efficiency explains the long-term effect of ecosystem engineers on primary production. Functional Ecology 21, 1–10.
Nutrient cycling efficiency explains the long-term effect of ecosystem engineers on primary production.Crossref | GoogleScholarGoogle Scholar |

Bernier N (1998) Earthworm feeding activity and development of the humus profile. Biology and Fertility of Soils 26, 215–223.
Earthworm feeding activity and development of the humus profile.Crossref | GoogleScholarGoogle Scholar |

Bhattacharjee G, Chaudhuri PS (2002) Cocoon production, morphology, hatching pattern and fecundity in seven tropical earthworm species: a laboratory-based investigation. Journal of Biosciences 27, 283–294.
Cocoon production, morphology, hatching pattern and fecundity in seven tropical earthworm species: a laboratory-based investigation.Crossref | GoogleScholarGoogle Scholar | 12089477PubMed |

Blouin M, Hodson ME, Delgado EA, Baker G, Brussaard L, Butt KR, Dai J, Dendooven L, Peres G, Tondoh JE, Cluzeau D, Brun JJ (2013) A review of earthworm impact on soil function and ecosystem services. European Journal of Soil Science 64, 161–182.
A review of earthworm impact on soil function and ecosystem services.Crossref | GoogleScholarGoogle Scholar |

Brossard M, Lavelle P, Laurent JY (1996) Digestion of a vertisol by the endogeic earthworm Polypheretima elongata, megascolecidae, increases soil phosphate extractability. European Journal of Soil Biology 32, 107–111.

Chapuis-Lardy L, Brossard M, Lavelle P, Schouller E (1998) Phosphorus transformations in a ferralsol through ingestion by Pontoscolex corethrurus, a geophagous earthworm. European Journal of Soil Biology 34, 61–67.
Phosphorus transformations in a ferralsol through ingestion by Pontoscolex corethrurus, a geophagous earthworm.Crossref | GoogleScholarGoogle Scholar |

Chapuis-Lardy L, Brauman A, Bernard L, Pablo AL, Toucet J, Mano MJ, Weber L, Brunet D, Razafimbelo T, Chotte JL, Blanchart E (2010) Effect of the endogeic earthworm Pontoscolex corethrurus on the microbial structure and activity related to CO2 and N2O fluxes from a tropical soil (Madagascar). Applied Soil Ecology 45, 201–208.
Effect of the endogeic earthworm Pontoscolex corethrurus on the microbial structure and activity related to CO2 and N2O fluxes from a tropical soil (Madagascar).Crossref | GoogleScholarGoogle Scholar |

Charlier JB, Cattan P, Voltz M, Moussa R (2009) Transport of a nematicide in surface and groundwater in a tropical volcanic catchment. Journal of Environmental Quality 38, 1031–1041.
Transport of a nematicide in surface and groundwater in a tropical volcanic catchment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVGiur8%3D&md5=9304497a01691cbc058422508c20ec5dCAS | 19329691PubMed |

Chaudhuri PS, Pal TK, Nath S, Dey SK (2012) Effects of five earthworm species on some physico-chemical properties of soil. Journal of Environmental Biology 33, 713–716.

Clermont-Dauphin C, Cabidoche YM, Meynard JM (2004) Effects of intensive monocropping of bananas on properties of volcanic soils in the uplands of the French West Indies. Soil Use and Management 20, 105–113.
Effects of intensive monocropping of bananas on properties of volcanic soils in the uplands of the French West Indies.Crossref | GoogleScholarGoogle Scholar |

Curry JP, Schmidt O (2007) The feeding ecology of earthworms – A review. Pedobiologia 50, 463–477.
The feeding ecology of earthworms – A review.Crossref | GoogleScholarGoogle Scholar |

d’Alexis S, Loranger-Merciris G, Mahieu M, Boval M (2009) Influence of earthworms on development of the free-living stages of gastrointestinal nematodes in goat faeces. Veterinary Parasitology 163, 171–174.
Influence of earthworms on development of the free-living stages of gastrointestinal nematodes in goat faeces.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1Mvhs12qsA%3D%3D&md5=100f6522c6d93ffdbaac111b82666e3bCAS | 19443123PubMed |

FAO/UNESCO (2006) ‘World reference base for soil resources.’ World Soil Resources Reports 103. (FAO: Rome)

Fissore C, Giardina CP, Kolka RK (2013) Reduced substrate supply limits the temperature response of soil organic carbon decomposition. Soil Biology & Biochemistry 67, 306–311.
Reduced substrate supply limits the temperature response of soil organic carbon decomposition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1CqtL7P&md5=01ed76aada96721fab2b54be6ba668b3CAS |

Fonte SJ, Six J (2010) Earthworms and litter management contributions to ecosystem services in a tropical agroforestry system. Ecological Applications 20, 1061–1073.
Earthworms and litter management contributions to ecosystem services in a tropical agroforestry system.Crossref | GoogleScholarGoogle Scholar | 20597290PubMed |

Jiménez JJ, Lal R (2006) Mechanisms of C sequestration in soils of Latin America. Critical Reviews in Plant Sciences 25, 337–365.
Mechanisms of C sequestration in soils of Latin America.Crossref | GoogleScholarGoogle Scholar |

Jouquet P, Bernard-Reversat F, Bottinelli N, Orange D, Rouland-Lefèvre C, Tran Duc T, Podwojewski P (2007) Influence of changes in land use and earthworm activities on carbon and nitrogen dynamics in a steepland ecosystem in Northern Vietnam. Biology and Fertility of Soils 44, 69–77.
Influence of changes in land use and earthworm activities on carbon and nitrogen dynamics in a steepland ecosystem in Northern Vietnam.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVGmt7zK&md5=ce0eec5a4d74ec9609ce8c97ab257d32CAS |

Jouquet P, Plumere T, Thu TD, Rumpel C, Duc TT, Orange D (2010) The rehabilitation of tropical soils using compost and vermicompost is affected by the presence of endogeic earthworms. Applied Soil Ecology 46, 125–133.
The rehabilitation of tropical soils using compost and vermicompost is affected by the presence of endogeic earthworms.Crossref | GoogleScholarGoogle Scholar |

Lafont A, Risède JM, Loranger-Merciris G, Clermont-Dauphin C, Dorel M, Rhino B, Lavelle P (2007) Effects of the earthworm Pontoscolex corethrurus on banana plants infected or not with the plant-parasitic nematode Radopholus similis. Pedobiologia 51, 311–318.
Effects of the earthworm Pontoscolex corethrurus on banana plants infected or not with the plant-parasitic nematode Radopholus similis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVGjurvP&md5=c072e0c9c9a9cbf9abd969fd323c7537CAS |

Lavelle P (2002) Functional domains in soils. Ecological Research 17, 441–450.
Functional domains in soils.Crossref | GoogleScholarGoogle Scholar |

Lavelle P, Spain AV (2001) ‘Soil ecology.’ (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Lavelle P, Pashanasi B, Charpentier F, Gilot C, Rossi JP, Derouard L, Andre J, Ponge JF, Bernier N (2004) Effects of earthworms on soil organic matter and nutrient dynamics at a landscape scale over decades. In ‘Eathworm ecology’. (Ed. CA Edwards) pp. 145–180. (CRC Press LLC: Boca Raton, FL, USA)

Lim SL, Wu TY, Sim EYS, Lim PN, Clarke C (2012) Biotransformation of rice husk into organic fertilizer through vermicomposting. Ecological Engineering 41, 60–64.
Biotransformation of rice husk into organic fertilizer through vermicomposting.Crossref | GoogleScholarGoogle Scholar |

Loranger-Merciris G, Cabidoche YM, Deloné B, Quénéhervé P, Ozier-Lafontaine H (2012) How earthworm activities affect banana plant response to nematode parasitism. Applied Soil Ecology 52, 1–8.
How earthworm activities affect banana plant response to nematode parasitism.Crossref | GoogleScholarGoogle Scholar |

Majeed E, Miambi E, Barois I, Blanchart E, Brauman A (2013) Emissions of nitrous oxide from casts of tropical earthworms belonging to different ecological categories. Pedobiologia 56, 49–58.
Emissions of nitrous oxide from casts of tropical earthworms belonging to different ecological categories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyjug%3D%3D&md5=e3675a7bd420ee90970ab9b3b415ad82CAS |

Marhan S, Scheu S (2005) Effects of sand and litter availability on organic matter decomposition in soil and in casts of Lumbricus terrestris L. Geoderma 128, 155–166.
Effects of sand and litter availability on organic matter decomposition in soil and in casts of Lumbricus terrestris L.Crossref | GoogleScholarGoogle Scholar |

McInerney M, Bolger T (2000) Temperature, wetting cycles and soil texture effects on carbon and nitrogen dynamics in stabilized earthworms casts. Soil Biology & Biochemistry 32, 335–349.
Temperature, wetting cycles and soil texture effects on carbon and nitrogen dynamics in stabilized earthworms casts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1Smt7w%3D&md5=f10bff58c40e21332cf67331dc2f2890CAS |

McInerney M, Little DJ, Bolger T (2001) Effect of earthworm cast formation on the stabilization of organic matter in fine soil fractions. European Journal of Soil Biology 37, 251–254.
Effect of earthworm cast formation on the stabilization of organic matter in fine soil fractions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsVGkurw%3D&md5=ac34b5fa5d106891c217eef8761eb0aeCAS |

Morel C, Fardeau JC (1987) Available phosphorus in intertropical soils: its relation with phosphorus determined by two extraction methods (Olsen, Olsen Dabin). Agronomie Tropicale 42, 248–257.

Pashanasi B, Lavelle P, Alegre J, Charpentier F (1996) Effect of the endogeic earthworm Pontoscolex corethrurus on soil chemical characteristics and plant growth in a low-input tropical agroecosystem. Soil Biology & Biochemistry 28, 801–810.
Effect of the endogeic earthworm Pontoscolex corethrurus on soil chemical characteristics and plant growth in a low-input tropical agroecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XktFalur4%3D&md5=14d8e2a604049752537c4da68c4bb5c1CAS |

SAS Institute (1999) ‘SAS User’s Guide.’ (SAS Institute: Cary, NC, USA)

Sheehan C, Kirwan L, Connolly J, Bolger T (2007) The effects of earthworm functional group diversity on earthworm community structure. Pedobiologia 50, 479–487.
The effects of earthworm functional group diversity on earthworm community structure.Crossref | GoogleScholarGoogle Scholar |

Shipitalo MJ, Le Bayon RC (2004) Quantifying the effects of earthworm on soil aggregation and porosity. Earthworm Ecology 10, 183–200.

Sierra J (2006) A hot-spot approach applied to nitrification in tropical acid soils. Soil Biology & Biochemistry 38, 644–652.
A hot-spot approach applied to nitrification in tropical acid soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivVaqsb8%3D&md5=36ae43d6d42385f926fc83d52b402aceCAS |

Sierra J, Dulormne M, Desfontaines L (2002) Soil nitrogen as affected by Gliricidia sepium in a silvopastoral system in Guadeloupe, French Antilles. Agroforestry Systems 54, 87–97.
Soil nitrogen as affected by Gliricidia sepium in a silvopastoral system in Guadeloupe, French Antilles.Crossref | GoogleScholarGoogle Scholar |

Sierra J, Brisson N, Ripoche D, Déqué M (2010) Modelling the impact of thermal adaptation of soil microorganisms and crop system on the dynamics of organic matter in a tropical soil under a climate change scenario. Ecological Modelling 221, 2850–2858.
Modelling the impact of thermal adaptation of soil microorganisms and crop system on the dynamics of organic matter in a tropical soil under a climate change scenario.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1ems7zL&md5=ab7d9e1b6fa76515a1c3515deca6c364CAS |

Sierra J, Desfontaines L, Faverial J, Loranger-Merciris G, Boval M (2013) Composting and vermicomposting of cattle manure and green wastes under tropical conditions: carbon and nutrient balances and end-product quality. Soil Research 51, 142–151.
Composting and vermicomposting of cattle manure and green wastes under tropical conditions: carbon and nutrient balances and end-product quality.Crossref | GoogleScholarGoogle Scholar |

Tabatabai MA (1994) Soil enzymes. In ‘Methods of soil analysis. Part 2: Microbiological and biochemical properties’. (Eds RW Weaver et al.) pp. 775–833. (Soil Science Society of America: Madison, WI, USA)

Tiquia SM (2005) Microbiological parameters as indicators of compost maturity. Journal of Applied Microbiology 99, 816–828.
Microbiological parameters as indicators of compost maturity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFyhsrrJ&md5=5d09f6617fdeeaf64c73916cf0435df8CAS | 16162232PubMed |