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Review on Control Methods Against Plant Parasitic Nematodes Applied in Southern Member States (C Zone) of the European Union agriculture Review Review on Control Methods against Plant Parasitic Nematodes Applied in Southern Member States (C Zone) of the European Union Nicola Sasanelli 1, Alena Konrat 2, Varvara Migunova 3,*, Ion Toderas 4, Elena Iurcu-Straistaru 4, Stefan Rusu 4, Alexei Bivol 4, Cristina Andoni 4 and Pasqua Veronico 1 1 Institute for Sustainable Plant Protection, CNR, St. G. Amendola 122/D, 70126 Bari, Italy; [email protected] (N.S.); [email protected] (P.V.) 2 Federal State Budget Scientific Institution “Federal Scientific Centre VIEV” (FSC VIEV) of RAS, Bolshaya Cheryomushkinskaya 28, 117218 Moscow, Russia; [email protected] 3 A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky Prospect 33, 119071 Moscow, Russia 4 Institute of Zoology, MECC, Str. Academiei 1, 2028 Chisinau, Moldova; [email protected] (I.T.); [email protected] (E.I.-S.); [email protected] (S.R.); [email protected] (A.B.); [email protected] (C.A.) * Correspondence: [email protected] Abstract: The European legislative on the use of different control strategies against plant-parasitic nematodes, with particular reference to pesticides, is constantly evolving, sometimes causing confu- Citation: Sasanelli, N.; Konrat, A.; sion in the sector operators. This article highlights the nematode control management allowed in the Migunova, V.; Toderas, I.; C Zone of the European Union, which includes the use of chemical nematicides (both fumigant and Iurcu-Straistaru, E.; Rusu, S.; Bivol, non-fumigant), agronomic control strategies (crop rotations, biofumigation, cover crops, soil amend- A.; Andoni, C.; Veronico, P. Review ments), the physical method of soil solarization, the application of biopesticides (fungi, bacteria and on Control Methods against Plant their derivatives) and plant-derived formulations. The authors analyze the use of these strategies Parasitic Nematodes Applied in and substances in organic agriculture as well as in Integrated Pest Management (IPM) programs. Southern Member States (C Zone) of the European Union. Agriculture 2021, 11, 602. https://doi.org/10.3390/ Keywords: biopesticides; chemicals; EU legislation; nematode control strategies; plant extracts agriculture11070602 Academic Editors: Sarah J. Pethybridge and Frank Hay 1. Introduction Plant-parasitic nematodes (PPNs) can severely damage plants and cause significant Received: 4 June 2021 yield losses to numerous vegetable crops [1–3]. The degree of plant growth impairment Accepted: 24 June 2021 caused by PPNs may depend on the nematode species, physiological race and the initial Published: 28 June 2021 nematode population density in the soil at sowing or transplanting. In the case of high levels of soil infestation (>64 eggs and juveniles/mL soil), they can completely destroy Publisher’s Note: MDPI stays neutral the crop as the plants may die [1]. They can interact with soilborne plant pathogens with regard to jurisdictional claims in causing greater severity of symptoms (yellowing, stunting growth, wilting, dwarfism) of published maps and institutional affil- plant disease [4–6]. Seinhorst’s equation y = m + (1 − m) z(P−T) describes the relationship iations. between nematode population density and crops (Figure1)[ 7,8]. Therefore, nematode control strategies are required to limit nematode population density to no-damage levels. The latest European Legislations (Reg. (EU) 2005/396; 2007/1095; 2009/1107; 2016/2031; 2019/1702; 2019/2072; EC Directives 2009/127 and 128) have been deeply revised and Copyright: © 2021 by the authors. restricted the use of pesticides on agricultural crops focusing attention on environmental Licensee MDPI, Basel, Switzerland. safety, human and animal health. Plant protection strategies against PPNs, insects and This article is an open access article soil-borne plant pathogens should therefore rely on alternative control measures that are distributed under the terms and both environmentally sound and economically sustainable. conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Agriculture 2021, 11, 602. https://doi.org/10.3390/agriculture11070602 https://www.mdpi.com/journal/agriculture Agriculture 2021, 11, 602 2 of 19 Agriculture 2021, 11, 602 2 of 19 Figure 1. RelationshipRelationship between plantplant growthgrowth [plant[plant weight weight (black) (black) and and height height (white)] (white)] and and nematode nematodepopulation population density in density the soil representedin the soil represen by Seinhort’sted by equation.Seinhort’s Inequation. this equation, In thisy equation,(relative yield)y (relativeis the ratio yield) of the is the yield ratio at of a giventhe yield population at a given density populationPi to thedensity yield Pi in to the the absence yield in ofthe nematodes, absence ofm nematodes,is the minimum m is the relative minimum yield relative (y at very yield large (y atPi ),veryz is large a constant Pi), z is < a 1, constant where z -T< 1,= where 1.05; Pi z-Tis = the 1.05;nematode Pi is the population nematode density population at transplant density at or transplant sowing and orT sowingis the tolerance and T is the limit tolerance of the crop limit to of the thenematode crop to (thePi at nematode which no (Pi yield at which is lost). no yield is lost). TheIn the latest past, anEuropean effective nematodeLegislations control (Reg. was (EU) achieved 2005/396; by the 2007/1095; use of methyl 2009/1107; bromide 2016/2031;(MB). The use201 of9/1702; this product 2019/2072; has beenEC Dire bannedctives in 2009/127 advanced and countries 128) have since 2005been becausedeeply revisedof stratospheric and restricted ozone the depletion. use of Afterpesticides the ban on onagricultural the use of crops MB and focusing the revocation attention of on 1, environmental3-dichloropropene safety, in Europeanhuman and Union animal (EU) health. countries, Plant theprotection control strategies strategies against aim to reducePPNs, insectssoil nematode and soil-borne population plant levels pathogens to below the shou toleranceld therefore threshold rely of on the alternative crop; they integrate control measureschemical nematicides,that are both bionematicidesenvironmentally (mainly sound basedand economically on fungi orbacteria), sustainable. physical meth- ods (soilIn the solarization, past, an effective heating nematode sterilization, control ozone was treatments) achieved by and/or the use agronomic of methyl practicesbromide (MB).(crop rotation,The use of use this of product resistant has varieties been bann or nematicidaled in advanced plants, countries anaerobic since soil 2005 disinfection, because ofgreen stratospheric manures, biofumigation,ozone depletion. soil After amendments). the ban on the use of MB and the revocation of 1, 3-dichloropropeneThe registration in European process for Union pesticides (EU) countries, in the EU the starts control with strategies the active aim ingredient to reduce soilapproval nematode process population which ends levels with ato vote, below after the which, tolerance when positive,threshold the of active the crop; is listed they in integrateAnnex 1 aschemical approved. nematicides, For the authorization bionematicides of formulated (mainly products,based on afterfungi Annex or bacteria), 1 listing physicalof active substancesmethods (soil and theirsolarization, use, the EUheating is divided sterilization, into three ozone zones: treatments) A—North Europeand/or agronomic(Denmark, Estonia,practices Finland,(crop rotation, Latvia, Lithuania,use of resistant Sweden), varieties B—Central or nematicidal Europe (Austria, plants, anaerobicBelgium, Croatia,soil disinfection, Czech Republic, green manure Germany,s, biofumigation, Ireland, The Netherlands, soil amendments). Poland, Romania, SlovakThe Republic, registration Slovenia, process Hungary) for pesticides and C—South in the EU Europe starts with (Bulgaria, the active Cyprus, ingredient France, approvalGreece, Italy, process Malta, which Portugal ends with and a Spain) vote, after [Reg. which, (EU) when 2009/1107]. positive, The the evaluation active is listed and inapproval Annex of1 aas pesticide approved. ornematicide For the authorization product can beof doneformulated at a zonal products, level and after later Annex follows 1 listingthe national of active registrations substances in and the their countries use, the of theEU zone.is divided Considering into three that zones: the A—North European Europelegislation (Denmark, on the use Estonia, of pesticides Finland, is constantly Latvia, Lithuania, evolving, sometimes Sweden), causingB—Central confusion Europe in (Austria,sector operators, Belgium, this Croatia, paper Czech reports Republic, the nematode Germany, control Ireland, methods The appliedNetherlands, in the Poland, C Zone Romania,of the EU. Slovak These includeRepublic, the Slovenia, use of fumigants Hungary) and and systemic C—South nematicides, Europe (Bulgaria, agronomic Cyprus, and France,physical Greece, methods, Italy, biopesticides Malta, Portugal and plantand Spain) extracts, [Reg. omitting (EU) 2009/1107]. some of the The most evaluation obvious andtechniques approval such of a as pesticide the use ofor resistantnematicide cultivars product or can the be grafting done at of a susceptible zonal level plantsand later on followsresistant the rootstocks. national registrations in the countries of the zone. Considering that the European2. Fumigants legislation on the use of pesticides is constantly
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