agronomy Article The Efficacy of Seed Treatments on Major Sugar Beet Pests: Possible Consequences of the Recent Neonicotinoid Ban Helena Viric Gasparic 1,* , Darija Lemic 1 , Zrinka Drmic 2 , Maja Cacija 1 and Renata Bazok 1 1 Department of Agricultural Zoology, Faculty of Agriculture, University of Zagreb, Svetosimunska 25, 10000 Zagreb, Croatia; [email protected] (D.L.); [email protected] (M.C.); [email protected] (R.B.) 2 Croatian Agency for Agriculture and Food, VinkovaˇckaStreet 63c, 31000 Osijek, Croatia; [email protected] * Correspondence: [email protected]; Tel.: +385-12393804 Abstract: Sugar beet production remains unprotected after the ban on neonicotinoids, while pest pressure is increasing. Although the organic approach to agriculture is highly welcomed, the question remains whether it will be possible to grow sugar beet without pesticides. The aim of this study is to determine the efficacy of seed treatments with neonicotinoids on the main sugar beet pests, to determine the susceptibility of the pests under the specific climatic conditions and to discuss possible consequences of the ban of neonicotinoids on the future of sugar beet production in southeast Europe. The study was conducted in two different climatic regions in Croatia in two consecutive years. The tested variants were: seed coated with imidacloprid, seed coated with a combination of thiamethoxam and teflutrin and untreated control. Our results showed that seed coatings with imidacloprid and thiamethoxam provided satisfactory protection against wireworms, flea beetles and sugar beet weevils at low population pressure. These pests are regular pests of sugar beet in southern Citation: Viric Gasparic, H.; Lemic, and eastern Europe and therefore need to be controlled. Caterpillars and aphids were present in low D.; Drmic, Z.; Cacija, M.; Bazok, R. populations, so the efficacy of the insecticides tested cannot be determined with certainty. A further The Efficacy of Seed Treatments on research program is needed to find alternative solutions and develop easily implementable strategies Major Sugar Beet Pests: Possible for all sugar beet pests. We would propose an authorization of neonicotinoids for seed treatment of Consequences of the Recent sugar beet in the regions with high infestation pressure of the main sugar beet pests. Neonicotinoid Ban. Agronomy 2021, 11, 1277. https://doi.org/10.3390/ Keywords: efficacy; imidacloprid; insect pests; thiametoxam; teflutrin; seed agronomy11071277 Academic Editor: Ivo Toševski 1. Introduction Received: 29 April 2021 According to Kristek et al. [1], sugar beet is a profitable industrial crop grown com- Accepted: 22 June 2021 Published: 23 June 2021 mercially for sugar production. It is grown in Europe over approximately 2,000,000 ha, which is about 70% of the total arable land in the world. In the Republic of Croatia, sugar Publisher’s Note: MDPI stays neutral represents an important export product. Until 2012, it was grown on 23,215 ha with an with regard to jurisdictional claims in average yield of 50.95 t/ha [1]. In recent years, sugar beet production has decreased not published maps and institutional affil- only in Croatia, but in all countries of the EU. For example, in 2018, sugar beet yield per iations. hectare decreased by 15% compared to 2017 [2]. Croatian sugar beet production in 2018 was reduced by 40%, which means up to 524 thousand tons compared to the production of the previous year [3]. Sugar beet has a long growing season of up to 200 days, during which it can be exposed to many diseases, insect pests and fungal diseases [4]. According to Meier et al. [5], Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. phenological growth stages are defined as follows: Germination from 00-dry seed to This article is an open access article 09-emergence: shoot emerges through the soil surface; leaf development or youth stage distributed under the terms and from 10-first leaf visible: cotyledons unfolded horizontally to 19-nine and more leaves conditions of the Creative Commons unfolded; rosette growth (crop cover) from 31-beginning of crop cover: leaves cover 10% Attribution (CC BY) license (https:// of the ground to 39-crop cover complete: Leaves cover 90% of the ground; development of creativecommons.org/licenses/by/ harvestable vegetative plant parts is defined by code 49-Beet root has reached harvestable 4.0/). size. Other stages represent the appearance of inflorescences in the 2nd year of growth. Agronomy 2021, 11, 1277. https://doi.org/10.3390/agronomy11071277 https://www.mdpi.com/journal/agronomy Agronomy 2021, 11, 1277 2 of 16 Agronomy 2021, 11, 1277 2 of 15 size. Other stages represent the appearance of inflorescences in the 2nd year of growth. BBCH identificationBBCH codes identification are shown codes in areFigure shown 1. The in Figure decrease1. The in decrease production in production is due to is due to economic reasonseconomic and changing reasons climatic and changing cond climaticitions, which conditions, led to which major led problems to major problemsrelated related to the inability toto effectively the inability control to effectively pests. controlIn Croatia, pests. pests In Croatia, are a limiting pests are afactor limiting in sugar factor in sugar beet production beet[6]. production [6]. Figure 1.FigurePhenological 1. Phenological development development of sugar beet of plantssugar isbeet shown plants by using is shown BBCH by codes using as BBCH follows: codes 00 sowing as fol- (dry seed), 01–09 germination,lows: 00 sowing 10–19 (dry leaf development,seed), 01–09 germination, 31–39 rosette growth, 10–19 leaf and development, 49–development 31–39 of harvestable rosette growth, vegetative and plant parts (root),49 –development Meier et al., (1993). of harvestable vegetative plant parts (root), Meier et al., (1993). The most commonThe pests most that common attack pests sugar that beet attack insugar the early beet stages in the early of leaf stages development of leaf development or the youth stageor (BBCH the youth 10–19) stage and (BBCH cause 10–19) major and damage cause major are damagewireworms are wireworms (Agriotes (Agriotesspp., spp., Coleoptera: Elateridae), which live in the soil and feed on roots. The main damage occurs Coleoptera: Elateridae), which live in the soil and feed on roots. The main damage occurs in spring and is manifested by thinning of the crop stand and reduction in yield [7]. Flea in spring and is beetlesmanifested (Chaetocnema by thinning tibialis ofIll., th Coleoptera:e crop stand Chrysomelidae) and reduction cause in yield damage [7]. byFlea feeding on beetles (Chaetocnemaleaves tibialis and forming Ill., Coleoptera: small round Chrysomelidae) holes (1 mm in cause diameter) damage that by enlarge feeding as leaveson grow. leaves and formingSometimes small round they feed holes on the(1 mm stem in in diameter) addition to that the leavesenlarge [7 ].as When leaves the grow. plant is at the Sometimes they cotyledonfeed on the stage, stem one in flea addition can cause to 33%the leaves damage [7]. per When day, three the fleasplant up is toat 62%the and five cotyledon stage,fleas one canflea cause can cause as much 33% as 90%damage damage per today, the three plant. fleas Their up activity to 62% increases and five with higher fleas can cause astemperatures, much as 90% i.e., damage warmer to climate-more the plant. Their damage activity [8]. Sugar increases beet with weevils higher (Bothynoderes punctiventris Germ., Coleoptera: Curculionidae) emerge from the soil in early spring when temperatures, i.e., warmer climate-more damage [8]. Sugar◦ beet weevils (Bothynoderes punctiventris Germ.,the upperColeoptera: layer reaches Curculionidae) a temperature emerge of 6–10from C[the9 soil]. Normally, in early spring sugar beetswhen are at the cotyledon stage at this time, so the damage can be extensive. In one day, an adult weevil can the upper layer reaches a temperature of 6–10 °C [9]. Normally, sugar beets are at the consume up to 50% of the emerged plants in m2. Again, the insect’s feeding rate increases cotyledon stage withat this temperature. time, so the At damage 20 ◦C, an can adult be weevilextensive. eats In 34 one mm 2day,of leaf an area, adult while weevil at 32 ◦C the can consume uparea to 50% increases of the up emerged to 145 mm plants2 [8]. The in m2. caterpillars Again, of the noctuid insect’s moths feeding (Agrotis rate segetum in- Schiff., creases with temperature.Agrotis ypsilon At Hubn.20 °C, andan adultEuxoa weevil temera Hb., eats Lepidoptera: 34 mm2 of Noctuidae)leaf area, while can cause at 32 damage to °C the area increasesmore up than to 150 145 host mm2 plants. [8]. The firstcaterpillars generation of ofnoctuid caterpillars moths is the (Agrotis most damaging, segetum feeding Schiff., Agrotis ypsilonon underground Hubn. and and Euxoa aboveground temera Hb., parts Lepidoptera: of newly emerged Noctuidae) plants. Infestationcan cause can lead damage to more tothan thinning 150 host of the plants. crop standThe firs andt reducedgeneration yields. of caterpillars Often a caterpillar is the most can bite dam- off the plant ˇ aging, feeding onhaze. underground According to andCamprag abovegro [10],und 5–10 parts caterpillars of newly of the emerged species A. plants. ipsilon can Infes- damage 90% of plants up to 8 cm high. Later in vegetation, sugar beet can be attacked by several species tation can lead to thinning of the crop stand and reduced yields. Often a caterpillar can of aphids (Hemiptera: Aphididae) such as Smynthurodes phaseoli West, Pemphigus fuscicornis bite off the plantKoch haze. and AccordingPemphigus to betae ČampragDoane on[10], roots 5–10 and caterpillarsAphis fabae Scopoli of the andspeciesMyzus A. persicaeipsi- Sulzer lon can damage as90% the of most plants common up to species 8 cm onhigh. aboveground Later in vegetation, organs [11]. Insugar addition beet to can aphids, be at- caterpillars tacked by severalof species the rapeseed of aphids moth (Hemiptera: (Scrobipalpa ocellatella Aphididae)Boyd, such Lepidoptera: as Smynthurodes Gelechiidae), phaseoli the cabbage West, Pemphigusmoth fuscicornis and bright-line Koch and brown-eye Pemphigus moth betae (Mamestra Doane on brassicae roots andL.