Control biológico de enfermedades y plagas promovido por lombrices
Palavras-chave:
biocontrol, oligochaeta, manejo fitosanitario alternativoResumo
A pesar de vaivenes en la historia al respecto de cómo se ha interpretado la acción de las lombrices sobre el suelo y las plantas, actualmente se acepta como un hecho que estos anélidos tienen un efecto positivo indirecto sobre la productividad y sanidad vegetal, al mejorar las propiedades del suelo que sustenta la vida de las plantas. Lo que resulta más novedoso, quizás, es la acción directa que se ha descubierto que pueden tener las lombrices al suprimir ciertas plagas y enfermedades; o influyendo directamente sobre el sistema de defensa de las plantas. Estas líneas de investigación tienen varias décadas de desarrollo a nivel mundial, pero son muy poco conocidas en el mundo hispano-parlante, con escasa literatura en el tema escrita en español. La presente revisión pretende reunir los casos que han demostrado un efecto positivo significativo de las lombrices sobre la sanidad vegetal, indagar en los mecanismos por los cuales éstas pueden participar del control biológico de parástitos fitófagos o fitopatógenos, y discutir las perspectivas de aplicación del control biológico mediante el uso de lombrices como parte de una agricultura sustentable y agroecológica.Referências
AYUKE, F. O.; et al. Effects of biocontrol bacteria and earthworms on the severity of Alternaria brassicae disease
and the growth of oilseed rape plants (Brassica napus). Applied Soil Ecology, v 117, p. 63 – 69, 2017.
BERTRAND, M.; et al. Biocontrol of eyespot winter wheat fungal disease by an anecic earthworm Lumbricus
terrestris, L.) In: 13th ESA CONGRESS, 13, 25-29 August 2014, Debrecen, Hungary. Annals of event, 2014. p. 51 -52
BERTRAND, M.; et al. Biocontrol of eyespot disease on two winter wheat cultivars by an anecic earthworm
(Lumbricus terrestris). Applied Soil Ecology, v 96, p. 33-41, 2015.
BLOUIN, M.; et al. Belowground organism activities affect plant aboveground phenotype, including plant tolerance
to parasites. Ecology Letters, n. 8, p. 202-208, 2005.
BLOUIN, M.; et al. Earthworms (Millsonia anomala, Megascolecidae) do not increase rice growth through enhanced
nitrogen mineralization. Soil Biology & Biochemistry, v. 38, p. 2063–2068, 2006.
BLOUIN, M.; et al. A review of earthworm impact on soil function and ecosystem services. European Journal of Soil
Science, v. 62, n. 4, p. 161–182, 2013.
BONKOWSKI, S.; et al. Food preference of earthworms for soil fungi. Pedobiologia. v. 44, p. 666–676, 2000.
BOUCHÉ, M.B. Strategies lombriciennes. Ecological Bulletins, Soil Organisms as Components of Ecosystems, v. 25,
p. 122-132, 1977.
BOYER, J.; et al. Effects of trefoil cover crop and earthworm inoculation on maize crop and soil organisms in
Reunion Island. Biology & Fertility of Soils, v. 28, n.4, p. 364–370, 1999.
BOYER J.; et al. Interactions between earthworms and plant-parasitic nematodes. European Journal of Soil Biology,
v. 59, p. 43-47, 2013.
BROWN, G. G.; et al. Effects of Earthworms on Plant Production in the Tropic. In: LAVELLE, P.; BRUSSAARD, L.;
HENDRIX, P. (Org.) Earthworm Management in Tropical Agroecosystems. Wallingford-New York: CAB.
International, 1999. p. 87-147.
BROWN, G. G.; et al. How earthworms affect plant growth: Burrowing into the mechanisms. In: Edwards C.A.
(Org.). Earthworm ecology (2nd ed). London: Boca Raton: CRC Press, 2004. p. 19–49.
BROWN, G. G. How do earthworms affect microfloral and faunal community diversity? Plant & Soil, v. 170, n. 1, p.
209–231, 1995.
CAMACHO VALDEZ, V.; RUIZ LUNA, A. Marco conceptual y clasificación de los servicios ecosistémicos. Revista Bio
Ciencias, v. 1, n. 4, p. 3-15, 2012.
CANELLAS, L. P.; et al. Probing the hormonal activity of fractionated molecular humic components in tomato auxin
mutants. Annals of Applied Biology, p. 1-10, 2011.
CHO, J. H.; et al. Lumbricin I, a novel proline-rich antimicrobial peptide from the earthworm: purification, cDNA
cloning and molecular characterization. Biochimica et Biophysica Acta, v. 1408, p. 67-76, 1998.
CLAPPERTON, M. J.; et al. Earthworms indirectly reduce the effects of take-all (Gaeumannomyces
graminis var. tritici) on soft white spring wheat (Triticum aestivum cv. Fielder). Soil Biology & Biochemistry, v. 33,
n. 11, p. 1531-1538, 2001.
CUNHA, L; et al. Soil animals and pedogenesis: The role of earthworms in anthropogenic soils. Soil Science (E), v.:
181, p.: 110 - 125, 2016.
DE LA PEÑA, E. Efectos de la biota edáfica en las interacciones planta-insecto a nivel foliar. Ecosistemas, v. 18, n. 2,
p. 64-78, 2009.
DOUBE, B. M.; et al. Interactions between earthworms, beneficial soil microorganisms and root pathogens. Applied
Soil Ecology, v. 1, p. 3-10, 1994.
EDWARDS, C. A.; FLETCHER, K. E. Interactions between Earthworms and Microorganisms in Organic-matter
Breakdown. Agriculture, Ecosystems & Environment, v. 24, p. 235-247, 1988.
EDWARDS, C. A.; BOHLEN, P.J. The biology and ecology of earthworms. London: Chapman and Hall, 1996. 426p.
EDWARDS, C. A. Earthworm ecology (2nd ed). London: Boca Raton: CRC Press, 2004.424 p.
EDWARDS, C. A.; et al. The influence of vermicomposts on plant growth and pest incidence. In: SOIL ZOOLOGY FOR
SUSTAINABLE DEVELOPMENT IN THE 2IST CENTURY, 2004, Cairo. Resumen de trabajos presentados, Cairo: [s.n.]
Shakir, S.H. Hanna; Mikhaïl, W.Z.A. (Org.), 2004. p.397-420.
EILENBERG, J.; et al. Suggestions for unifying the terminology in biological control. BioControl, v. 46, p. 387-400,
2001.
ELLENBY, C. Influence of earthworms on larval emergence in the potato-root eelworm, Heterodra rostochiensis
Wollenweber, Annals of Applied Biology, v. 31, p. 332-339, 1945.
ELMER, W. H. Influence of earthworm activity on soil microbes and soilborne diseases of vegetables. Plant Disease,
v. 93, n. 2, p. 175–179, 2009.
FRIBERG, H.; et al. Influence of soil fauna on fungal plant pathogens in agricultural and horticultural systems.
Biocontrol Science & Technology, v. 15, n. 7, p. 641-658, 2005.
HASNA, M. K.; et al. Effects of fungivorous nematodes on corky-root disease of tomato grown in compost amended
soil. Acta Agriculture Scandinavica, Section B., Plant & Soil Science, v. 58, p. 145-153, 2008.
HIRST, J. M.; STEDMAN, O. J. The epidemiology of apple scab (Venturia inequalis (Cke) Wint). Annals of Applied
Biology, v. 50, p. 551-567, 1962.
HUME, E. A.; et al. Alleviation of takeall in wheat by the earthworm Aporrectodea caliginosa (Savigny). Applied Soil
Ecology, v. 90, p. 18–25, 2015.
ILIEVA-MAKULEC, K.; MAKULEC, G. Does the activity of the earthworm Aporrectodea caliginosa modify the plant
diversity effect on soil nematodes? European Journal of Soil Biology, v. 43, p. 157–164, 2007.
INFANTE-RODRÍGUEZ, D. A.; et al. Earthworm mediated dispersal of baculovirus occlusion bodies: Experimental
evidence from a model system. Biological Control, v. 100, p. 18–24, 2016.
JANA, U.; et al. Earthworms influence the production of above- and belowground biomass and the expression of
genes involved in cell proliferation and stress responses in Arabidopsis thaliana. Soil Biology & Biochemistry, v. 42,
p. 244–252, 2010.
JAYASINGHE, B. A. T. D.; PARKINSON, D. Earthworms as the vectors of actinomycetes antagonistic to litter
decomposer fungi. Applied Soil Ecology, v. 43, p.1–10, 2009.
JOHNSON, D. L.; SCHAETZL, R. J. Differing views of soil and pedogenesis by two masters: Darwin and Dokuchaev.
Geoderma. p. 237–238, 2015.
JONES, C. G.; et al. Organisms as ecosystem engineers. Oikos, v. 69, p. 373-386, 1994.
JORGE-ESCUDERO, G.; et al. Contribution of anecic and epigeic earthworms to biological control of Fusarium
graminearum in wheat straw. S/p.
KENNEL, W. The role of the earthworm Lumbricus terrestris in integrated fruit production, Acta Horticulturae, v.
285, p. 149-156, 1990.
LAFONT, A.; et al. Effects of the earthworm Pontoscolex corethrurus on banana plants infected or not with the
plant-parasitic nematode Radopholus similis. Pedobiologia, v. 51, p. 311–318, 2007.
LAGERLÖF, J.; et al. Potential side effects of biocontrol and plant-growth promoting Bacillus amyloliquefaciens
bacteria on earthworms. Applied Soil Ecology, v. 96, p. 159 – 164, 2015.
LAGERLÖF, J.; et al. Interaction between a fungal plant disease, fungivorous nematodes and compost
suppressiveness. Acta Agriculture Scandinavica Section B – Soil & Plant Science, v. 61, p. 372-377, 2011.
LAGERLÖF, J.; et al. Earthworms influenced by reduced tillage, conventional tillage and energy forest in Swedish
agricultural field experiments. Acta Agriculture Scandinavica Section B – Soil & Plant Science, v. 62, p. 235-244,
2012.
LAING, J. E.; et al. Leaf burial by the earthworm, Lumbricus terrestris (Oligochaeta: Lumbricidae), as a major factor
in the population dynamics of Phyllonorycter blancardella (Lepidoptera: Gracillariidae) and its parasites.
Environmental Entomology, v. 15, p. 321-326, 1986.
LAVELLE, P. Earthworm activities and the soil system. Biology & Fertility of Soils, v. 6, p. 237-251, 1988.
LAVELLE, P. Faunal activities and soil processes: Adaptive strategies that determine ecosystem function. Advances
in Ecological Research, v. 27, p. 93–132, 1997.
LAVELLE, P.; SPAIN A. V. Soil ecology. Boston-Massachusetts: Kluwer Academic, 2001. 654pp.
LEE, K. Earthworms: Their Ecology and Relationships with Soils and Land Use. New York: Academic Press, 1985.
411p.
LOHMANN, M.; et al. Decomposers and root feeders interactively affect plant defence in Sinapis alba. Oecologia, v.
160, p. 289–298, 2009.
MEGHVANSI, M. K.; et al. Assessing the Role of Earthworms in Biocontrol of Soil-Borne Plant Fungal Diseases. In:
Ayten Karaca (Org.) Biology of Earthworms. Noida, UP: Springer, 2011. p. 173-190.
MONTECCHIO, L.; et al. Potential spread of forest soil-borne fungi through earthworm consumption and casting.
iForest (early view): e1-e7, 2014.
MOODY, S.; et al. Fate of some fungal spores associated with wheat straw decomposition on passage through the
guts of Lumbricus terrestris and Aporrectodea longa. Soil Bioliology & Biochemistry, v. 28, n.4/5, p. 533-537. 1996.
NAKAMURA, Y.; et al. Influence of the earthworm Pheretima hilgendorfi (Megascolecidae) on Plasmodiophora
brassicae clubroot galls of cabbage seedlings in pot. Edaphologia, v. 54, p. 39-41, 1995.
NAKAMURA, Y. Interactions between earthworms and microorganisms in biological control of plant root
pathogens. Farming Japan, v. 30, n. 6, p. 37-43, 1996.
NEWINGTON, J. E.; et al. Potential Effects of Earthworms on Leaf-Chewer Performance. Functional Ecology, v. 18,
n. 5, p. 746-751, 2004.
NIKLAS, J.; KENNEL, W. The role of the earthworm, Lumbricus terrestris (L.) in removing sources of phytopathogenic
fungi in orchards, Gartenbauwissenschaft, v. 46, p. 138-142, 1981.
OLDENBURG, E.; et al. Impact of the earthworm Lumbricus terrestris on the degradation of Fusarium-infected and
deoxynivalenol-contaminated wheat straw. Soil Biology & Biochemistry, v. 40, p. 3049-3053, 2008.
POVEDA, K.; et al. Effects of decomposers and herbivores on plant performance and aboveground plant–insect
interactions. Oikos, v. 108, p. 503–510, 2005.
PUGA-FREITAS, R.; et al. Signal molecules mediate the impact of the earthworm Aporrectodea caliginosa on
growth, development and defence of the plant Arabidopsis thaliana. Plos One, v. 7, n. 12, p. 1-10, 2012a.
PUGA-FREITAS, R.; et al. Transcriptional profiling of wheat in response to take-all disease and mechanisms involved
in earthworm’s biocontrol effect. European Journal of Plant Pathology, v. 144, p. 155–165, 2016.
PUGA-FREITAS, R.; et al. Control of Cultivable IAA-producing bacteria by the plant Arabidopsis thaliana and the
earthworm Aporrectodea caliginosa. Applied & Environmental Soil Science, p. 1-4, 2012b.
RAW, F. Studies of earthworm populations in orchards. Annals of Applied Biology, v. 50, p. 389-404, 1962.
RUESS, L.; et al. Food preference of a fungal-feeding Aphelenchoides species. Nematology, v. 2, p. 223-230, 2000.
SCHEU, S. Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia, v. 47, p. 846–856,
2003.
SCHIEDECK, G.; et al. Densidade e biomassa de minhocas em pomar de pessegueiro sob diferentes manejos do solo.
Revista Brasileira de Agroecologia, v. 4, n. 2, p. 2725-2728, 2009a.
SCHIEDECK, G.; et al. Percepção de agricultores sobre o papel das minhocas nos agroecossistemas. Revista Brasileira
de Agroecologia, v. 4, n. 2, p. 856-859, 2009b.
SCHRADER, S.; et al. Biological control of soil-borne phytopathogenic fungi and their mycotoxins by soil fauna. A
review. Bulletin UASMV serie Agriculture, v. 70, n. 29, p. 291-298, 2013.
SENAPATI, B.K. Biotic interactions between soil nematodes and earthworms. Soil Biology & Biochemistry, v. 24, p.
1441–1444, 1992.
SHIPITALO, J. M.; LE BAYON, R. C. Quantifying the Effects of Earthworms on Soil Aggregation and Porosity. In:
Edwards C. A. (Org.), Earthworm ecology (2nd ed). London: Boca Raton: CRC Press, 2004. p. 19–49.
SIMSEK-ERSAHIN, Y. The Use of Vermicompost Products to Control Plant Diseases and Pests. In: Ayten Karaca (Org.)
Biology of Earthworms. Noida, UP: Springer, 2011. p. 191-214.
SINGER, A. C.; et al. Use of an anecic earthworm, Pheretima hawayana, as a means for delivery of fungal biocontrol
agents. Pedobiologia, v. 43, p. 771-775, 1999.
STEPHENS, P. M.; et al. Reduced severity of Rhizoctonia solani disease on wheat seedlings associated with the
presence of the earthworm Aporrectodea trapezoides Lumbricidae). Soil Biology & Biochemistry, v. 25, p. 1477-
1484, 1993.
STEPHENS, P. M.; et al. Influence of the earthworms Aporrectodea rosea and Aporrectodea trapezoides on
Rhizoctonia disease of wheat seedlings and the interaction with a surface mulch of cereal/pea straw. Soil Biology &
Biochemistry, v. 26, p. 1285-1287, 1994a.
STEPHENS, P. M.; et al. Field evidence for reduced severity of Rhizoctonia bare patch disease of wheat, due to the
presence of the earthworms Aporrectodea rosea and Aporrectodea trapezoides. Soil Biology & Biochemistry, v. 26,
p. 1495-1500, 1994b.
STEPHENS, P. M.; et al. Ability of the lumbricid earthworms Aporrectodea rosea and A. trapezoides to reduce the
severity of take-all under greenhouse and field conditions. Soil Biology & Biochemistry, v. 26, p. 1291-1297, 1994c
STEPHENS, P. M.; DAVOREN, C. W. Effect of the lumbricid earthworm Aporrectodea trapezoides on wheat grain
yield in the field, presence or absence of Rhizoctonia solani and Gaumannomyces graminis var tritici. Soil Biology &
Biochemistry, v. 33, n.11, p. 1531–1538, 1995.
STEPHENS, P. M.; DAVOREN, C. W. Influence of the earthworm Aporrectodea trapezoides and A. rosea on the
disease severity of Rhizoctonia solani on subterranean clover and ryegrass. Soil Biology & Biochemistry, v. 29, p.
511-516, 1997.
TAO, J.; et al. Earthworms change the abundance and community structure of nematodes and protozoa in a maize
residue amended rice–wheat rotation agro-ecosystem. Soil Biology & Biochemistry, v. 41, p. 898–904, 2009.
TOYOTA, K.; KIMURA, M. Earthworms disseminate a soil-borne plant pathogen, Fusarium oxysporum f. sp. Raphani.
Biology & Fertility of Soils, v. 18, p. 32-36, 1994.
VAN GROENIGEN, J. W.; et al. Earthworms increase plant production: a meta-analysis. Scientific Reports-Nature, v.
4, p. 1-7, 2014.
WANG, C.; et al. A novel antimicrobial vermipeptide family from earthworm Eisenia fetida. European Journal of
Soil Biology, v. 43, p. 127-134, 2007.
WANG, C.; et al. Function of mucilaginous secretions in the antibacterial immunity system of Eisenia fetida.
Pedobiologia, v. 54, p.57–62, 2011.
WARDLE, D.A.; et al. Linking Aboveground and Belowground Communities: The Indirect Influence of Aphid Species
Identity and Diversity on a Three Trophic Level Soil Food Web. Oikos, v. 107, n. 2, p. 283-294, 2004.
WOLFARTH, F.; et al. Earthworms promote the reduction of Fusarium biomass and deoxynivalenol content in
wheat straw under field conditions. Soil Biology & Biochemistry, v. 43, p. 1858-1865, 2011a.
WOLFARTH, F.; et al. Contribution of the endogeic earthworm species Aporrectodea caliginosa to the degradation
of deoxynivalenol and Fusarium biomass in wheat straw. Mycotoxin Research, v. 27, p. 215–220, 2011b.
WURST, S.; et al. Effects of earthworms and organic litter distribution on plant performance and aphid
reproduction. Oecologia, v. 137, p. 90–96, 2003.
WURST, S.; et al. Combined effects of earthworms and vesicular-arbuscular mycorrhizas on plant and aphid
performance. New Phytologist, v. 163, p. 169–176, 2004.
WURST, S.; et al. Effects of belowground biota on primary and secondary metabolites in Brassica oleracea.
Chemoecology, v. 16, p. 69–73, 2006.
WURST, S.; et al. Earthworms counterbalance the negative effect of microorganisms on plant diversity and enhance
the tolerance of grasses to nematodes. Oikos, v. 117, p. 711–718, 2008.
WURST, S. Effects of earthworms on above- and belowground herbivores. Applied Soil Ecology, v. 45, p. 123–130,
2010.
YEATES, G.W. Influence of earthworms on soil nematode populations. Annual Abstracts Society of Nematologists,
Journal of Nematology, v. 12, n. 4, p. 242-242, 1980.
YEATES, G.W. Soil nematode populations depressed in the presence of earthworms. Pedobiologia, v. 22, p. 191–
195, 1981.
ZERBINO, M.S. Evaluación de la densidad, biomasa y diversidad de la macrofauna del suelo en diferentes
sistemas de producción. 92p. Tesis (Maestría en Ciencias Ambientales) - Facultad de Ciencias, Universidad de la
República, Montevideo, 2005.
ZERBINO M.S.; et al. Evaluación de la macrofauna del suelo en sistemas de producción en siembra directa y con
pastoreo. Agrociencia (Uruguay), v. 1, p. 44-55, 2008.
ZERBINO M.S. Evaluación de la macrofauna del suelo en rotaciones cultivo-pasturas con laboreo convencional.
Acta Zoológica Mexicana, 26:189-202, 2010.
and the growth of oilseed rape plants (Brassica napus). Applied Soil Ecology, v 117, p. 63 – 69, 2017.
BERTRAND, M.; et al. Biocontrol of eyespot winter wheat fungal disease by an anecic earthworm Lumbricus
terrestris, L.) In: 13th ESA CONGRESS, 13, 25-29 August 2014, Debrecen, Hungary. Annals of event, 2014. p. 51 -52
BERTRAND, M.; et al. Biocontrol of eyespot disease on two winter wheat cultivars by an anecic earthworm
(Lumbricus terrestris). Applied Soil Ecology, v 96, p. 33-41, 2015.
BLOUIN, M.; et al. Belowground organism activities affect plant aboveground phenotype, including plant tolerance
to parasites. Ecology Letters, n. 8, p. 202-208, 2005.
BLOUIN, M.; et al. Earthworms (Millsonia anomala, Megascolecidae) do not increase rice growth through enhanced
nitrogen mineralization. Soil Biology & Biochemistry, v. 38, p. 2063–2068, 2006.
BLOUIN, M.; et al. A review of earthworm impact on soil function and ecosystem services. European Journal of Soil
Science, v. 62, n. 4, p. 161–182, 2013.
BONKOWSKI, S.; et al. Food preference of earthworms for soil fungi. Pedobiologia. v. 44, p. 666–676, 2000.
BOUCHÉ, M.B. Strategies lombriciennes. Ecological Bulletins, Soil Organisms as Components of Ecosystems, v. 25,
p. 122-132, 1977.
BOYER, J.; et al. Effects of trefoil cover crop and earthworm inoculation on maize crop and soil organisms in
Reunion Island. Biology & Fertility of Soils, v. 28, n.4, p. 364–370, 1999.
BOYER J.; et al. Interactions between earthworms and plant-parasitic nematodes. European Journal of Soil Biology,
v. 59, p. 43-47, 2013.
BROWN, G. G.; et al. Effects of Earthworms on Plant Production in the Tropic. In: LAVELLE, P.; BRUSSAARD, L.;
HENDRIX, P. (Org.) Earthworm Management in Tropical Agroecosystems. Wallingford-New York: CAB.
International, 1999. p. 87-147.
BROWN, G. G.; et al. How earthworms affect plant growth: Burrowing into the mechanisms. In: Edwards C.A.
(Org.). Earthworm ecology (2nd ed). London: Boca Raton: CRC Press, 2004. p. 19–49.
BROWN, G. G. How do earthworms affect microfloral and faunal community diversity? Plant & Soil, v. 170, n. 1, p.
209–231, 1995.
CAMACHO VALDEZ, V.; RUIZ LUNA, A. Marco conceptual y clasificación de los servicios ecosistémicos. Revista Bio
Ciencias, v. 1, n. 4, p. 3-15, 2012.
CANELLAS, L. P.; et al. Probing the hormonal activity of fractionated molecular humic components in tomato auxin
mutants. Annals of Applied Biology, p. 1-10, 2011.
CHO, J. H.; et al. Lumbricin I, a novel proline-rich antimicrobial peptide from the earthworm: purification, cDNA
cloning and molecular characterization. Biochimica et Biophysica Acta, v. 1408, p. 67-76, 1998.
CLAPPERTON, M. J.; et al. Earthworms indirectly reduce the effects of take-all (Gaeumannomyces
graminis var. tritici) on soft white spring wheat (Triticum aestivum cv. Fielder). Soil Biology & Biochemistry, v. 33,
n. 11, p. 1531-1538, 2001.
CUNHA, L; et al. Soil animals and pedogenesis: The role of earthworms in anthropogenic soils. Soil Science (E), v.:
181, p.: 110 - 125, 2016.
DE LA PEÑA, E. Efectos de la biota edáfica en las interacciones planta-insecto a nivel foliar. Ecosistemas, v. 18, n. 2,
p. 64-78, 2009.
DOUBE, B. M.; et al. Interactions between earthworms, beneficial soil microorganisms and root pathogens. Applied
Soil Ecology, v. 1, p. 3-10, 1994.
EDWARDS, C. A.; FLETCHER, K. E. Interactions between Earthworms and Microorganisms in Organic-matter
Breakdown. Agriculture, Ecosystems & Environment, v. 24, p. 235-247, 1988.
EDWARDS, C. A.; BOHLEN, P.J. The biology and ecology of earthworms. London: Chapman and Hall, 1996. 426p.
EDWARDS, C. A. Earthworm ecology (2nd ed). London: Boca Raton: CRC Press, 2004.424 p.
EDWARDS, C. A.; et al. The influence of vermicomposts on plant growth and pest incidence. In: SOIL ZOOLOGY FOR
SUSTAINABLE DEVELOPMENT IN THE 2IST CENTURY, 2004, Cairo. Resumen de trabajos presentados, Cairo: [s.n.]
Shakir, S.H. Hanna; Mikhaïl, W.Z.A. (Org.), 2004. p.397-420.
EILENBERG, J.; et al. Suggestions for unifying the terminology in biological control. BioControl, v. 46, p. 387-400,
2001.
ELLENBY, C. Influence of earthworms on larval emergence in the potato-root eelworm, Heterodra rostochiensis
Wollenweber, Annals of Applied Biology, v. 31, p. 332-339, 1945.
ELMER, W. H. Influence of earthworm activity on soil microbes and soilborne diseases of vegetables. Plant Disease,
v. 93, n. 2, p. 175–179, 2009.
FRIBERG, H.; et al. Influence of soil fauna on fungal plant pathogens in agricultural and horticultural systems.
Biocontrol Science & Technology, v. 15, n. 7, p. 641-658, 2005.
HASNA, M. K.; et al. Effects of fungivorous nematodes on corky-root disease of tomato grown in compost amended
soil. Acta Agriculture Scandinavica, Section B., Plant & Soil Science, v. 58, p. 145-153, 2008.
HIRST, J. M.; STEDMAN, O. J. The epidemiology of apple scab (Venturia inequalis (Cke) Wint). Annals of Applied
Biology, v. 50, p. 551-567, 1962.
HUME, E. A.; et al. Alleviation of takeall in wheat by the earthworm Aporrectodea caliginosa (Savigny). Applied Soil
Ecology, v. 90, p. 18–25, 2015.
ILIEVA-MAKULEC, K.; MAKULEC, G. Does the activity of the earthworm Aporrectodea caliginosa modify the plant
diversity effect on soil nematodes? European Journal of Soil Biology, v. 43, p. 157–164, 2007.
INFANTE-RODRÍGUEZ, D. A.; et al. Earthworm mediated dispersal of baculovirus occlusion bodies: Experimental
evidence from a model system. Biological Control, v. 100, p. 18–24, 2016.
JANA, U.; et al. Earthworms influence the production of above- and belowground biomass and the expression of
genes involved in cell proliferation and stress responses in Arabidopsis thaliana. Soil Biology & Biochemistry, v. 42,
p. 244–252, 2010.
JAYASINGHE, B. A. T. D.; PARKINSON, D. Earthworms as the vectors of actinomycetes antagonistic to litter
decomposer fungi. Applied Soil Ecology, v. 43, p.1–10, 2009.
JOHNSON, D. L.; SCHAETZL, R. J. Differing views of soil and pedogenesis by two masters: Darwin and Dokuchaev.
Geoderma. p. 237–238, 2015.
JONES, C. G.; et al. Organisms as ecosystem engineers. Oikos, v. 69, p. 373-386, 1994.
JORGE-ESCUDERO, G.; et al. Contribution of anecic and epigeic earthworms to biological control of Fusarium
graminearum in wheat straw. S/p.
KENNEL, W. The role of the earthworm Lumbricus terrestris in integrated fruit production, Acta Horticulturae, v.
285, p. 149-156, 1990.
LAFONT, A.; et al. Effects of the earthworm Pontoscolex corethrurus on banana plants infected or not with the
plant-parasitic nematode Radopholus similis. Pedobiologia, v. 51, p. 311–318, 2007.
LAGERLÖF, J.; et al. Potential side effects of biocontrol and plant-growth promoting Bacillus amyloliquefaciens
bacteria on earthworms. Applied Soil Ecology, v. 96, p. 159 – 164, 2015.
LAGERLÖF, J.; et al. Interaction between a fungal plant disease, fungivorous nematodes and compost
suppressiveness. Acta Agriculture Scandinavica Section B – Soil & Plant Science, v. 61, p. 372-377, 2011.
LAGERLÖF, J.; et al. Earthworms influenced by reduced tillage, conventional tillage and energy forest in Swedish
agricultural field experiments. Acta Agriculture Scandinavica Section B – Soil & Plant Science, v. 62, p. 235-244,
2012.
LAING, J. E.; et al. Leaf burial by the earthworm, Lumbricus terrestris (Oligochaeta: Lumbricidae), as a major factor
in the population dynamics of Phyllonorycter blancardella (Lepidoptera: Gracillariidae) and its parasites.
Environmental Entomology, v. 15, p. 321-326, 1986.
LAVELLE, P. Earthworm activities and the soil system. Biology & Fertility of Soils, v. 6, p. 237-251, 1988.
LAVELLE, P. Faunal activities and soil processes: Adaptive strategies that determine ecosystem function. Advances
in Ecological Research, v. 27, p. 93–132, 1997.
LAVELLE, P.; SPAIN A. V. Soil ecology. Boston-Massachusetts: Kluwer Academic, 2001. 654pp.
LEE, K. Earthworms: Their Ecology and Relationships with Soils and Land Use. New York: Academic Press, 1985.
411p.
LOHMANN, M.; et al. Decomposers and root feeders interactively affect plant defence in Sinapis alba. Oecologia, v.
160, p. 289–298, 2009.
MEGHVANSI, M. K.; et al. Assessing the Role of Earthworms in Biocontrol of Soil-Borne Plant Fungal Diseases. In:
Ayten Karaca (Org.) Biology of Earthworms. Noida, UP: Springer, 2011. p. 173-190.
MONTECCHIO, L.; et al. Potential spread of forest soil-borne fungi through earthworm consumption and casting.
iForest (early view): e1-e7, 2014.
MOODY, S.; et al. Fate of some fungal spores associated with wheat straw decomposition on passage through the
guts of Lumbricus terrestris and Aporrectodea longa. Soil Bioliology & Biochemistry, v. 28, n.4/5, p. 533-537. 1996.
NAKAMURA, Y.; et al. Influence of the earthworm Pheretima hilgendorfi (Megascolecidae) on Plasmodiophora
brassicae clubroot galls of cabbage seedlings in pot. Edaphologia, v. 54, p. 39-41, 1995.
NAKAMURA, Y. Interactions between earthworms and microorganisms in biological control of plant root
pathogens. Farming Japan, v. 30, n. 6, p. 37-43, 1996.
NEWINGTON, J. E.; et al. Potential Effects of Earthworms on Leaf-Chewer Performance. Functional Ecology, v. 18,
n. 5, p. 746-751, 2004.
NIKLAS, J.; KENNEL, W. The role of the earthworm, Lumbricus terrestris (L.) in removing sources of phytopathogenic
fungi in orchards, Gartenbauwissenschaft, v. 46, p. 138-142, 1981.
OLDENBURG, E.; et al. Impact of the earthworm Lumbricus terrestris on the degradation of Fusarium-infected and
deoxynivalenol-contaminated wheat straw. Soil Biology & Biochemistry, v. 40, p. 3049-3053, 2008.
POVEDA, K.; et al. Effects of decomposers and herbivores on plant performance and aboveground plant–insect
interactions. Oikos, v. 108, p. 503–510, 2005.
PUGA-FREITAS, R.; et al. Signal molecules mediate the impact of the earthworm Aporrectodea caliginosa on
growth, development and defence of the plant Arabidopsis thaliana. Plos One, v. 7, n. 12, p. 1-10, 2012a.
PUGA-FREITAS, R.; et al. Transcriptional profiling of wheat in response to take-all disease and mechanisms involved
in earthworm’s biocontrol effect. European Journal of Plant Pathology, v. 144, p. 155–165, 2016.
PUGA-FREITAS, R.; et al. Control of Cultivable IAA-producing bacteria by the plant Arabidopsis thaliana and the
earthworm Aporrectodea caliginosa. Applied & Environmental Soil Science, p. 1-4, 2012b.
RAW, F. Studies of earthworm populations in orchards. Annals of Applied Biology, v. 50, p. 389-404, 1962.
RUESS, L.; et al. Food preference of a fungal-feeding Aphelenchoides species. Nematology, v. 2, p. 223-230, 2000.
SCHEU, S. Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia, v. 47, p. 846–856,
2003.
SCHIEDECK, G.; et al. Densidade e biomassa de minhocas em pomar de pessegueiro sob diferentes manejos do solo.
Revista Brasileira de Agroecologia, v. 4, n. 2, p. 2725-2728, 2009a.
SCHIEDECK, G.; et al. Percepção de agricultores sobre o papel das minhocas nos agroecossistemas. Revista Brasileira
de Agroecologia, v. 4, n. 2, p. 856-859, 2009b.
SCHRADER, S.; et al. Biological control of soil-borne phytopathogenic fungi and their mycotoxins by soil fauna. A
review. Bulletin UASMV serie Agriculture, v. 70, n. 29, p. 291-298, 2013.
SENAPATI, B.K. Biotic interactions between soil nematodes and earthworms. Soil Biology & Biochemistry, v. 24, p.
1441–1444, 1992.
SHIPITALO, J. M.; LE BAYON, R. C. Quantifying the Effects of Earthworms on Soil Aggregation and Porosity. In:
Edwards C. A. (Org.), Earthworm ecology (2nd ed). London: Boca Raton: CRC Press, 2004. p. 19–49.
SIMSEK-ERSAHIN, Y. The Use of Vermicompost Products to Control Plant Diseases and Pests. In: Ayten Karaca (Org.)
Biology of Earthworms. Noida, UP: Springer, 2011. p. 191-214.
SINGER, A. C.; et al. Use of an anecic earthworm, Pheretima hawayana, as a means for delivery of fungal biocontrol
agents. Pedobiologia, v. 43, p. 771-775, 1999.
STEPHENS, P. M.; et al. Reduced severity of Rhizoctonia solani disease on wheat seedlings associated with the
presence of the earthworm Aporrectodea trapezoides Lumbricidae). Soil Biology & Biochemistry, v. 25, p. 1477-
1484, 1993.
STEPHENS, P. M.; et al. Influence of the earthworms Aporrectodea rosea and Aporrectodea trapezoides on
Rhizoctonia disease of wheat seedlings and the interaction with a surface mulch of cereal/pea straw. Soil Biology &
Biochemistry, v. 26, p. 1285-1287, 1994a.
STEPHENS, P. M.; et al. Field evidence for reduced severity of Rhizoctonia bare patch disease of wheat, due to the
presence of the earthworms Aporrectodea rosea and Aporrectodea trapezoides. Soil Biology & Biochemistry, v. 26,
p. 1495-1500, 1994b.
STEPHENS, P. M.; et al. Ability of the lumbricid earthworms Aporrectodea rosea and A. trapezoides to reduce the
severity of take-all under greenhouse and field conditions. Soil Biology & Biochemistry, v. 26, p. 1291-1297, 1994c
STEPHENS, P. M.; DAVOREN, C. W. Effect of the lumbricid earthworm Aporrectodea trapezoides on wheat grain
yield in the field, presence or absence of Rhizoctonia solani and Gaumannomyces graminis var tritici. Soil Biology &
Biochemistry, v. 33, n.11, p. 1531–1538, 1995.
STEPHENS, P. M.; DAVOREN, C. W. Influence of the earthworm Aporrectodea trapezoides and A. rosea on the
disease severity of Rhizoctonia solani on subterranean clover and ryegrass. Soil Biology & Biochemistry, v. 29, p.
511-516, 1997.
TAO, J.; et al. Earthworms change the abundance and community structure of nematodes and protozoa in a maize
residue amended rice–wheat rotation agro-ecosystem. Soil Biology & Biochemistry, v. 41, p. 898–904, 2009.
TOYOTA, K.; KIMURA, M. Earthworms disseminate a soil-borne plant pathogen, Fusarium oxysporum f. sp. Raphani.
Biology & Fertility of Soils, v. 18, p. 32-36, 1994.
VAN GROENIGEN, J. W.; et al. Earthworms increase plant production: a meta-analysis. Scientific Reports-Nature, v.
4, p. 1-7, 2014.
WANG, C.; et al. A novel antimicrobial vermipeptide family from earthworm Eisenia fetida. European Journal of
Soil Biology, v. 43, p. 127-134, 2007.
WANG, C.; et al. Function of mucilaginous secretions in the antibacterial immunity system of Eisenia fetida.
Pedobiologia, v. 54, p.57–62, 2011.
WARDLE, D.A.; et al. Linking Aboveground and Belowground Communities: The Indirect Influence of Aphid Species
Identity and Diversity on a Three Trophic Level Soil Food Web. Oikos, v. 107, n. 2, p. 283-294, 2004.
WOLFARTH, F.; et al. Earthworms promote the reduction of Fusarium biomass and deoxynivalenol content in
wheat straw under field conditions. Soil Biology & Biochemistry, v. 43, p. 1858-1865, 2011a.
WOLFARTH, F.; et al. Contribution of the endogeic earthworm species Aporrectodea caliginosa to the degradation
of deoxynivalenol and Fusarium biomass in wheat straw. Mycotoxin Research, v. 27, p. 215–220, 2011b.
WURST, S.; et al. Effects of earthworms and organic litter distribution on plant performance and aphid
reproduction. Oecologia, v. 137, p. 90–96, 2003.
WURST, S.; et al. Combined effects of earthworms and vesicular-arbuscular mycorrhizas on plant and aphid
performance. New Phytologist, v. 163, p. 169–176, 2004.
WURST, S.; et al. Effects of belowground biota on primary and secondary metabolites in Brassica oleracea.
Chemoecology, v. 16, p. 69–73, 2006.
WURST, S.; et al. Earthworms counterbalance the negative effect of microorganisms on plant diversity and enhance
the tolerance of grasses to nematodes. Oikos, v. 117, p. 711–718, 2008.
WURST, S. Effects of earthworms on above- and belowground herbivores. Applied Soil Ecology, v. 45, p. 123–130,
2010.
YEATES, G.W. Influence of earthworms on soil nematode populations. Annual Abstracts Society of Nematologists,
Journal of Nematology, v. 12, n. 4, p. 242-242, 1980.
YEATES, G.W. Soil nematode populations depressed in the presence of earthworms. Pedobiologia, v. 22, p. 191–
195, 1981.
ZERBINO, M.S. Evaluación de la densidad, biomasa y diversidad de la macrofauna del suelo en diferentes
sistemas de producción. 92p. Tesis (Maestría en Ciencias Ambientales) - Facultad de Ciencias, Universidad de la
República, Montevideo, 2005.
ZERBINO M.S.; et al. Evaluación de la macrofauna del suelo en sistemas de producción en siembra directa y con
pastoreo. Agrociencia (Uruguay), v. 1, p. 44-55, 2008.
ZERBINO M.S. Evaluación de la macrofauna del suelo en rotaciones cultivo-pasturas con laboreo convencional.
Acta Zoológica Mexicana, 26:189-202, 2010.
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Control biológico de enfermedades y plagas promovido por lombrices. (2018). Revista Brasileira De Agroecologia, 13(4). https://revista.aba-agroecologia.org.br/rba/article/view/22530
