Abstract
Aims
Biofumigation, the burying of Brassicaceaous plant tissues to suppress soil pests, is an increasingly practiced technique. However, the efficiency of biofumigation varies considerably and motivated our meta-analysis on the topic.
Methods
We meta-analyzed data from 46 publications where 934 experiments used 363 unique controls, in order to determine effectiveness of this practice compared with untreated controls, and to identify which aspects of treatment regimens were most important for ensuring success.
Conclusions
Biofumigation generally reduced pest abundance, reduced incidence of disease, and increased crop yield by 30% over values seen in untreated controls. Neither the plant part incorporated, nor the method used to incorporate it, were important predictors of success. Contrary to our expectations, we found no evidence that solarization was beneficial, and only treatment regimens without solarization were generally effective. While treatment regimens varied, the most effective treatment combination that we identified was the incorporation of young Eruca and Raphanus plants, with high glucosinolate concentrations, applied at high doses with short exposure times to suppress the nematode Globodera in Solanaceous plants. Each component of this regimen would likely increase the effectiveness of biofumigation efforts aimed at other soil pests.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ITCs:
-
Isothiocyanates
References
Ahuja I, Rohloff J, Bones A (2010) Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for integrated pest management. A review. Agron Sustain Dev 30:311–348. https://doi.org/10.1051/agro/2009025
Aires A, Carvalho R, Barbosa M, Rosa E (2009) Suppressing potato cyst nematode, Globodera rostochiensis, with extracts of Brassicacea plants. Am J Potato Res 86:327–333. https://doi.org/10.1007/s12230-009-9086-y
Barto EK, Rillig MC (2012) Dissemination biases in ecology: effect sizes matter more than quality. Oikos 121:228–235
Barto EK, Friese CF, Cipollini D (2010) Arbuscular mycorrhizal fungi protect a native plant from allelopathic effects of an invader. J Chem Ecol 36:351–360
Bohinc T, Ban S, Ban D, Trdan S (2012) Glucosinolates in plant protection strategies: a review. Arch Biol Sci 64:821–828. https://doi.org/10.2298/ABS1203821B
Bones AM, Rossiter JT (1996) The myrosinase-glucosinolate system, its organisation and biochemistry. Physiol Plant 97:194–208
Brown P, Morra M (1997) Control of soil-borne plant pests using glucosinolate-containing plants. Adv Agron 61(61):167–231. https://doi.org/10.1016/S0065-2113(08)60664-1
Chen YG, Olson DM, Ruberson JR (2010) Effects of nitrogen fertilization on tritrophic interactions. Arthropod Plant Interact 4:81–94. https://doi.org/10.1007/s11829-010-9092-5
Core Team R (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Doheny-Adams T, Lilley C, Barker A, Ellis S, Wade R, Atkinson H, Urwin P, Redeker K, Hartley S (2018) Constant isothiocyanate-release potentials across biofumigant seeding rates. J Agric Food Chem 66:5108–5116. https://doi.org/10.1021/acs.jafc.7b04610
Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463. https://doi.org/10.1111/j.0006-341X.2000.00455.x
Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51
Fourie H, Ahuja P, Lammers J, Daneel M (2016) Brassicaceae-based management strategies as an alternative to combat nematode pests: a synopsis. Crop Prot 80:21–41. https://doi.org/10.1016/j.cropro.2015.10.026
Gareau BJ (2010) A critical review of the successful CFC phase-out versus the delayed methyl bromide phase-out in the Montreal protocol. Int Environ Agreement Politics Law Econ 10:209–231. https://doi.org/10.1007/s10784-010-9120-z
Gimsing A, Kirkegaard J (2009) Glucosinolates and biofumigation: fate of glucosinolates and their hydrolysis products in soil. Phytochem Rev 8:299–310. https://doi.org/10.1007/s11101-008-9105-5
Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156
Henderson D, Riga E, Ramirez R, Wilson J, Snyder E (2009) Mustard biofumigation disrupts biological control by Steinernema spp. nematodes in the soil. Biol Control 48:316–322. https://doi.org/10.1016/j.biocontrol.2008.12.004
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425
Kirkegaard JA, Sarwar M (1998) Biofumigation potential of brassicas. I. Variation in glucosinolate profiles of diverse field-grown brassicas. Plant Soil 201:71–89
Koron D, Sonjak S, Regvar M (2014) Effects of non-chemical soil fumigant treatments on root colonisation with arbuscular mycorrhizal fungi and strawberry fruit production. Crop Prot 55:35–41. https://doi.org/10.1016/j.cropro.2013.09.009
Lajeunesse MJ (2011) On the meta-analysis of response ratios for studies with correlated and multi-group designs. Ecology 92:2049–2055. https://doi.org/10.1890/11-0423.1
Lazzeri L, Baruzzi G, Malaguti L, Antoniacci L (2003) Replacing methyl bromide in annual strawberry production with glucosinolate-containing green manure crops. Pest Manag Sci 59:983–990. https://doi.org/10.1002/ps.726
Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115. https://doi.org/10.2307/2680124
Lopez-Perez JA, Roubtsova T, Garcia MD, Ploeg A (2010) The potential of five winter-grown crops to reduce root-knot nematode damage and increase yield of tomato. J Nematol 42:120–127
Lord J, Lazzeri L, Atkinson H, Urwin P (2011) Biofumigation for control of pale potato cyst nematodes: activity of Brassica leaf extracts and green manures on Globodera pallida in vitro and in soil. J Agric Food Chem 59:7882–7890. https://doi.org/10.1021/jf200925k
Martin F (2003) Development of alternative strategies for management of soilborne pathogens currently controlled with methyl bromide. Annu Rev Phytopathol 41:325–350. https://doi.org/10.1146/annurev.phyto.41.052002.095514
Matthiessen J, Kirkegaard J (2006) Biofumigation and enhanced biodegradation: opportunity and challenge in soilborne pest and disease management. Crit Rev Plant Sci 25:235–265. https://doi.org/10.1080/07352680600611543
Meyer D, Zeileis A, Hornik K (2006) The Strucplot framework: visualizing multi-way contingency tables with vcd. J Stat Softw 17:1–48
Meyer D, Zeileis A, Hornik K (2017) vcd: Visualizing categorical data. R package version 1.4–4
Mocali S, Landi S, Curto G, Dallavalle E, Infantino A, Colzi C, d'Errico G, Roversi P, D'Avino L, Lazzeri L (2015) Resilience of soil microbial and nematode communities after biofumigant treatment with defatted seed meals. Ind Crop Prod 75:79–90. https://doi.org/10.1016/j.indcrop.2015.04.031
Morra MJ, Kirkegaard JA (2002) Isothiocyanate release from soil-incorporated Brassica tissues. Soil Biol Biochem 34:1683–1690
Motisi N, Montfort F, Dore T, Romillac N, Lucas P (2009) Duration of control of two soilborne pathogens following incorporation of above- and below-ground residues of Brassica juncea into soil. Plant Pathol 58:470–478. https://doi.org/10.1111/j.1365-3059.2008.02017.x
Motisi N, Poggi S, Filipe JAN, Lucas P, Dore T, Montfort F, Gilligan CA, Bailey DJ (2013) Epidemiological analysis of the effects of biofumigation for biological control of root rot in sugar beet. Plant Pathol 62:69–78. https://doi.org/10.1111/j.1365-3059.2012.02618.x
New M (1987) Feed and feeding of fish and shrimp. A manual on the preparation and presentation of compound feeds for shrimp and fish in aquaculture. Food and Agriculture Organization of the United Nations, Rome, Italy
Njoroge S, Riley M, Keinath A (2008) Effect of incorporation of Brassica spp. residues on population densities of soilborne microorganisms and on damping-off and Fusarium wilt of watermelon. Plant Dis 92:287–294. https://doi.org/10.1094/PDIS-92-2-0287
Nordin A, Strengbom J, Ericson L (2006) Responses to ammonium and nitrate additions by boreal plants and their natural enemies. Environ Pollut 141:167–174. https://doi.org/10.1016/j.envpol.2005.08.017
Oz H, Coskan A, Atilgan A (2017) Determination of effects of various plastic covers and biofumigation on soil temperature and soil nitrogen form in greenhouse solarization: New solarization cover material. J Polym Environ 25:370–377. https://doi.org/10.1007/s10924-016-0819-y
Piccinini E, Ferrari V, Campanelli G, Fusari F, Righetti L, Matteo R, Lazzeri L (2015) Effect of two bio-based liquid formulations from Brassica carinata in containing red spider mite (Tetranychus urticae) on eggplant. Ind Crop Prod 75:36–41. https://doi.org/10.1016/j.indcrop.2015.05.060
Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588. https://doi.org/10.1111/j.1469-8137.2009.02830.x
Rasmann S, Agrawal AA (2009) Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Curr Opin Plant Biol 12:473–478. https://doi.org/10.1016/j.pbi.2009.05.005
Reardon C, Strauss S, Mazzola M (2013) Changes in available nitrogen and nematode abundance in response to Brassica seed meal amendment of orchard soil. Soil Biol Biochem 57:22–29. https://doi.org/10.1016/j.soilbio.2012.10.011
Rios P, Gonzalez M, Obregon S, Carbonero MD, Leal JR, Fernandez P, De-Haro A, Sanchez ME (2017) Brassica-based seedmeal biofumigation to control Phytophthora cinnamomi in the Spanish "dehesa" oak trees. Phytopathol Mediterr 56:392–399. https://doi.org/10.14601/Phytopathol_Mediterr-20771
Rudolph R, Sams C, Steiner R, Thomas S, Walker S, Uchanski M (2015) Biofumigation performance of four Brassica crops in a green Chile pepper (Capsicum annuum) rotation system in southern New Mexico. Hortscience 50:247–253
Rudolph R, Zasada I, Hesse C, DeVetter L (2019) Brassicaceous seed meal, root removal, and chemical fumigation vary in their effects on soil quality parameters and Pratylenchus penetrans in a replanted floricane raspberry production system. Appl Soil Ecol 133:44–51. https://doi.org/10.1016/j.apsoil.2018.08.024
Smith B, Kirkegaard J, Howe G (2004) Impacts of Brassica break-crops on soil biology and yield of following wheat crops. Aust J Agric Res 55:1–11. https://doi.org/10.1071/AR03104
Snoeijers SS, Perez-Garcia A, Joosten M, De Wit P (2000) The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. Eur J Plant Pathol 106:493–506. https://doi.org/10.1023/a:1008720704105
Stevens CJ, David TI, Storkey J (2018) Atmospheric nitrogen deposition in terrestrial ecosystems: its impact on plant communities and consequences across trophic levels. Funct Ecol 32:1757–1769. https://doi.org/10.1111/1365-2435.13063
Thompson S, Sharp S (1999) Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med 18:2693–2708. https://doi.org/10.1002/(SICI)1097-0258(19991030)18:20<2693::AID-SIM235>3.0.CO;2-V
Throop HL, Lerdau MT (2004) Effects of nitrogen deposition on insect herbivory: implications for community and ecosystem processes. Ecosystems 7:109–133. https://doi.org/10.1007/s10021-003-0225-x
van Dam NM, Tytgat TOG, Kirkegaard JA (2009) Root and shoot glucosinolates: a comparison of their diversity, function and interactions in natural and managed ecosystems. Phytochem Rev 8:171–186. https://doi.org/10.1007/s11101-008-9101-9
Veresoglou SD, Barto EK, Menexes G, Rillig MC (2013) Fertilization affects severity of disease caused by fungal plant pathogens. Plant Pathol 62:961–969. https://doi.org/10.1111/ppa.12014
Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48
Viechtbauer W, Cheung MWL (2010) Outlier and influence diagnostics for meta-analysis. Res Synth Methods 1:112–125. https://doi.org/10.1002/jrsm.11
Weerakoon DMN, Reardon CL, Paulitz TC, Izzo AD, Mazzola M (2012) Long-term suppression of Pythium abappressorium induced by Brassica juncea seed meal amendment is biologically mediated. Soil Biol Biochem 51:44–52. https://doi.org/10.1016/j.soilbio.2012.03.027
Zasada IA, Halbrendt JM, Kokalis-Burelle N, LaMondia J, McKenry MV, Noling JW (2010) Managing nematodes without methyl bromide. Annu Rev Phytopathol 48(48):311–328. https://doi.org/10.1146/annurev-phyto-073009-114425
Acknowledgments
Comments from three anonymous reviewers substantially improved this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Anton Wasson .
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 744 kb)
Rights and permissions
About this article
Cite this article
Morris, E.K., Fletcher, R. & Veresoglou, S.D. Effective methods of biofumigation: a meta-analysis. Plant Soil 446, 379–392 (2020). https://doi.org/10.1007/s11104-019-04352-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-019-04352-y