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ProEnvironment

ProEnvironment 11 (2018) 170-179

Original Article

Efficacy of Pheromone Traps/Yellow and Blue Sticky Panels and other Biological Methods to Fight against Western flower Thrips at Offer Madsen Gartneriet A/S Glamsbjerg, Denmark

VARGA Melinda, Ion OLTEAN*, Teodora FLORIAN

University of Agricultural Sciences and Veterinary Medicine, Faculty of Agriculture, 3-5 Mănăștur Str., 400372 Cluj-Napoca, Romania

Received 11 August 2018; received and revised form 5 September 2018; accepted 9 September 2018 Available online 30 September 2018

Abstract

Many chemical and biological options exist to help manage pests and maintain healthy, productive garden plants, green plats, decorative flowers. Understanding some of the differences between chemical and biological alternatives can help to choose the best pest management approach for the problems at hand. Since the 1970s Frankliniella occidentalis has successfully invaded many countries to become one of the most important agricultural pests of ornamental, vegetable and fruit crops globally. Its invasiveness is largely attributed to the international movement of plant material and insecticide resistance, both of which have combined to foster the rapid spread of the species throughout the world. Individuals are very small and they reside in concealed places on plants; thus are easily hidden and hard to detect in transported plant material. They reproduce rapidly and are highly polyphagous, breeding on many horticultural crops that are transported around the world. Because this pest is causing a lot of damages in protected areas but also in open spaces is very important to find the more efficient methode to combate. This pest has raised great problems, and in order to prevent we used biological methods like natural predators (Amblyseius cucumeris and swirski) Nematoder, Nemazal and yellow sticky blue sticky traps. Aim of this study is to define the efficiency against Heliothrips haemorrhoidalis and Frankliniella occidentalis of the biological methods like use of natural predators, Nematoder treatments, Nemazal, pheromonal traps and use of colored traps in a protected area in Denmark, at Gartneriet Offer Madsen A/S, to analyze differences between simple glued yellow and blue traps and a combination of this with pheromone traps.

Keywords: damages, frowers, health, pests.

1. Introduction Greenhouses may be used to overcome Greenhouses allow for greater control over the shortcomings in the growing qualities of a piece of growing environment of plants. Depending upon the land, such as a short growing season or poor light technical specification of a greenhouse, key factors levels, and they can thereby improve food production which may be controlled include temperature, levels in marginal environments. Due the too much demand of light and shade, irrigation, fertilizer application, for flowers, cut and potted, as well as fresh vegetables and atmospheric humidity. throughout the year, a series of special buildings protected areas such as greenhouses [19, 22], solariums, and orchards are needed. * Corresponding author. Tel: +40-264-596384 All this protected areas are not able to provide Fax: +40-264-593792 a pest or disease free production, because of this is e-mail: [email protected] very important to establish strategies for pest control.

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This pest control can be chemical [4, 18, 44], such as cucumbers, capsicums, biological [7, 10, 31, 48, 52-54, 56], physical, chrysanthemums, Gerbera, roses, Saintpaulia and mechanical, etc. [19, 32, 56]. tomatoes. In southern Europe it is extremely The most important and commun pest in this damaging too many field crops, including capsicums, protected areas are: the greenhouse whiteflys, tomatoes, strawberries, table grapes and artichokes, Trialeurodes vaporariorum [2, 6, 31, 37, 41], the and at least in southern Italy, it has become a tobacco fly Bemisia tabaci [13, 27, 30, 43, 51, 55], dominant member of the thrips fauna in wild flowers. the leaf mining Tuta absoluta [9, 12, 20, 23, 26, 49], Similarly, in Kenya the species has become a the common red spider Tetranychus urticae [16, 34, dominant member of the wild thrips fauna near 39, 45, 46], the Calfornian trips- Frankliniella agricultural fields. In contrast, in Australia it has not occidentalis [1, 3, 8, 11, 15, 21, 29, 33, 50], been found breeding on any native plant species. Heliothrips hamemorrhoidalis [14, 35, 40, 47]. Damages. With their mouth parts, thrips Pest description. The adult of Frankliniella puncture individual plant cells, mostly in the occidentalis has a slender, flattened body, about 1 epidermis, and suck up their sap. The empty, air- mm (male) (0.039 inch) and 1.5 mm (female) (0.06 filled tissue causes the plant surface to get a inch) in length. There are three color forms, pale characteristic silvery appearance. Heavier yellow, intermediate and dark brown. The four infestations will lead to browning and wilting of leaf wings, in rest folded lengthwise, consist for the most tips, in extreme cases to shoot distortions and part of fringes. At their feet the have bladder dropping of leaves. When fruits or vegetables are like adhesive organs which allow them to walk on attacked, scarring can occur. Distinctive black spots extremely smooth surfaces [15, 17, 26, 28, 38]. of frass are left at the feeding sites. Lifecycle. Thrips have an unusual form of Egg-laying causes unsightly suberised marks incomplete metamorphosis. There are four nymphal due to the plant's reaction. F. occidentalis is strongly instars. They are all mobile, but only the first two, attracted to brightly colored flowers, which will actually called larvae, are able to ingest food. The consequently show discolored spots and become third and fourth are called prepupa and pupa, deformed; buds may fail to open. Ornamentals will respectively. Development is largely dependent on thus be gravely blemished and rendered temperature. Hatching occurs about 3-4 days after the unmarketable. In other crops, even more important egg has been laid, the nymphal stage can last from 5 than the direct damage as described is that by to 20 days. Adults are mature about 3 days after transmitted diseases. F. occidentalis is an important emerging, they can live up to 30 days. F. occidentalis vector of Tospoviruses, namely of Tomato spotted is facultative parthenogenetic. In warm regions or in wilt virus, which can cause severe reduction in greenhouses, where continuous breeding is possible, quality and yield of many crops. In persons it can have up to 12-15 generations per year. repeatedly exposed to great numbers of the insects Otherwise, adults and pupae will overwinter in skin and respiratory irritations have occasionally sheltered places like under lumps of soil, tree bark, in been observed. grass and weeds etc., and only one or two generations Prevention and control. In order to establish may be completed. In spring, the adults migrate to strategies for pest control it is extremely important to flowering plants and start with oviposition. The know the structure of the phytopathogens and their female lays about 40-50 eggs, 1-2 per day. Each is numerical density evolution. Integrated pest inserted singly into the plant tissue in a way that part management must continually change to meet pest of it remains protruding. All thrips are poor fliers, but management challenges [5, 24, 36, 42]. IPM is a easily transported passively by the wind. continuum that will change with time. The origin of F. occidentalis is in North Every farmer practices some type of IPM, as America. In the 1980s it was by chance introduced to long as they make progress in management. Starting Europe. Meanwhile, it has been spread with from the concept that integrated pest management international trade throughout subtropical and have to ensure a very low level of pesticides waste temperate regions of the world. production we have to take in consideration the Host plants. As a pest it is found both outdoors relationship between useful entomofauna and and in glasshouses, and it attacks flowers, fruits and harmful species. For this reason it is necessary to leaves of a wide range of cultivated plants. These establish a monitoring system of biodiversity for each include apples, apricots, peaches, nectarines and culture and also to choose the best pest control plums, roses, chrysanthemums, carnations, sweet combat method. peas, Gladiolus, Impatiens, Gerbera and Ranunculu Many tactics keep pest populations off-balance s, peas, tomatoes, capsicums, cucumbers, melons, and avoids development of resistance to pesticides. strawberries, lucerne, grapes and cotton. In northern Least-toxic effective methods are used before more Europe it is found particularly on glasshouse crops, toxic ones whenever possible.

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Cultural methods are suppress pest Most chemical controls are fast acting and problems by minimizing the conditions they need effective. They often offer control over many to live (water, shelter, food). Planting plants that different insects at once and the various life stages of are adapted to different kind of growing different pests. Biological control methods use living conditions, planting them in the right place, organisms such as natural predators, parasites and giving proper attention to their water and pathogens to control pest populations. They include nutritional needs. Strong plants resist diseases, beneficial bugs, such as lady beetles and parasitic outgrow weeds and are less likely to succumb to wasps, which prey on harmful insects. insects. Many beneficial insects are commercially Physical methods prevent pest access to available, and they can quickly reduce pests to the host or area, or, if the pests are already manageable levels. Biological pesticides are based on present, physically removing them by some naturally occurring organisms that prove toxic for means. For example, this could mean using certain insects. Chemical controls are often barriers, traps, vacuuming, mowing or tillage, inexpensive and readily available. While chemical depending upon the pest and situation. controls are often effective, they are usually seasonal Genetic methods to use pest-resistant plant and require reapplication with each growing season. varieties developed by classical plant breeding. Biological controls may take longer to deliver the Biological methods are use of predators, desired results, but the benefits can last well beyond parasites and diseases of pests in a targeted way your initial investment. Many chemical pesticides to suppress pest populations. persist in the environment, and pest populations can Chemical methods. There are many build up resistance to chemicals over time. However, "chemicals" that are used in pest management many invasive pests were imported and lack natural situations, but not all chemicals are alike from the predators in their new environment, making standpoint of their range of action, toxicity, or biological control challenging in some cases. The persistence in the environment. Biorational best options for controlling garden pests often chemicals are those that are less universally toxic combine a combination of chemical and biological and target a specific aspect of pest biology. An controls. This approach is known as integrated pest example might be diatomaceous earth used to management or IPM. It focuses on combining scratch the surface of insects to dehydrate them, methods to effectively control pests, while keeping or microbial pesticides that affect only a specific the environmental impact as low as possible. Dense group of insects. There are some biorational pest infestations may require the potency of chemical chemical tactics that are hard to classify by controls, but IPM uses them as a last resort. Even toxicity or that are used together in innovative natural pesticides may be powerful poisons, so ways with other tactics. always wear protective clothing, gloves and An example of this would be protective eyewear when working with pesticides, pheromones used together with sticky traps. whether chemical or biological. Pheromones are the chemicals produced by insects to attract their mates, and so these 2. Material and Method substances are not toxic. But they can be used in large amounts to "confuse" the mating process or There are at least 6,000 species of trips in the to attract insects to a trap. Other examples of such world. This pest is causing a lot of damages chemicals are repellants, attractants, and especially in protected areas, but they are present also antifeeding agents. Conventional pesticides in open spaces in different type of cultures.This study currently refers to synthetically produced has been made in 2017 from January until December compounds that act as direct toxins (nerve in Denmark at Gartneriet Offer Madsen A/S. This poisons, stomach poisons, etc.) There are many greenhouse exists for 5 generations. Initially it began new classes of chemicals being added to the older in 1880 as an old farmland. Thomas Offer Madsen conventional pesticides. Chemical pesticides, often took over this land of approximately 8,000 square based on man-made substances, are designed to meters on which he built some tomato greenhouses. reduce the vitality of pest populations. The most In 1965 this affair was taken over by Affa Offer usual methods are chemical and biological methods. Madsen's father, Thomas Offer Madsen. He has Chemical controls eradicate common pests in several replaced the idea of cultivating tomatoes with tulips. different ways. Some kill pests as soon as they come Since then the main production has been tulips in contact with the chemical. Others disrupt the pest's marketed as cut flowers. By the 1980s, he introduced ability to reproduce. Other chemical controls limit a fern culture, marketed as flower in pots because physical growth or influence pest behavior in ways tulips offered only at a certain time of the year, only detrimental to their lives. in 1996 went to Hoya. In 2000 this business was

172 VARGA Melinda et al./ProEnvironment 11(2018) 170-179 taken over by Thomas Offer Madsen, which production was three kind of Hoya ssp. As a method continues with the production of Hoya, but thanks to of control we used biological methods such as natural the market's demands in summer introduces 2 new predators Amblyseius cucumeris and swirski, cultures: daisies and Atlantis. The surface of the treatments with Nematoder almost weekly and as greenhouse has grown over these years from 8,000 sq well we made treatments with Neemazal. Neemazal m to 18,000 sq m. In 2004 a new branch, culture in is a broad spectrum botanical insecticide derived ceramics, was introduced, both succulent plants from the Neem seed kernel. It is used especially purchased from Spain, and Tillandsii from against aphids. Quatemala. In 2011, the main floral plants in this The azadirachtin compound from NeemAzal- greenhouse are Hoya australis and Hoya compacta T/S is produced by an exclusive patented aqueous and a production of Atlantis and in 2012 also a extraction process, resulting in a purified active production of chili and daisy. ingredient. NeemAzal-T/S can replace or improve Starting from 2013 beside the main production traditional chemical treatments and is beneficial for of Hoya australis and compact also had daisy both organic and conventional farming. The product production and chilly, and from 2016 also a prevents insecticide resistance due to its numerous (> production of cactus.Throughout 2017, weekly we 60) active ingredients. The product does not contain monitored a full greenhouse with 81 tables, choosing aflatoxins and solvent residues. Does not harm 16 tables to report the presence of the thrips, the main beneficial insects and predators. There is no evidence pest of Hoya compacta and Hoya australis, because of acute toxicity or reproductive effects obtained in of this we choose the house in what the main valid studies.

Figure 1. Production of Hoya ssp. with the pheromone traps (original)

Figure 2. Production of daisy (original)

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Figure 3. Production of chilly (original)

Sticky traps are quite valuable to growers 3. Results and Discussions especially in greenhouses, but they can also be used easily in outdoor crops. They are used for trapping or The monitoring has been made weekly but in monitoring. Putting traps out in numbers can be order to be easier to follow we ordered them by effective in reducing airborn ault population of months. certain pests like whiteflies and fungus gnats by All the monthly captures are in Table 1. trapping them. If used at the rate of one trap per 250 In the last week of 2016 were founded 46 square feet though- or one per 100 square feet in individuals on the yellow panels. larger or monoculture greenhouses- and checked, In the first week of 2017, 44 individuals were pests counted, on a regular schedule, changed as captured. In order to control the pest, we performed needed, and the results charted, sticky traps can be an 3 treatments with Nematoder using 250 ml in 500 l of effective monitoring tool. Sticky traps must be placed water. In weeks 2 and 3, the number of catches was 1-2 inches above plant vegetation so that the bottom close to those in the first week, respectively 68 and of the trap is just above the plants. 48 individuals, repeating treatment with Nematoder During a full year we monitored thrips this time using 500 ml in 200 l of water, and also we population in Offer Madsen Gartneriet in the same placed natural predators, 27 pcs/table. From week 4- location, named ”house’’ checking all the time the 9, the number of pests dropped significantly from 33 same number of tables, a total number of 16 from 81. to 14 individuals. On the rest of the table because of a big number of Although treatments have proven to be very thrips we placed just simple sticky panels. The aim of effective, but the treatment with Nematoder has been this project it was to find the best biological method repeated weekly. which could be used in case of big thrips population At week 10-12 the number of individuals attack. Biological methods used in this project were: started to increase again from 30 to 58 at week 12, two kind of sticky traps yellowed and blue colored, so we increased the dose of Nematoder treatment by pheromonal traps, Nematoder, Neemazal and natural performing 2 or even 3 treatments at week 12, and we predator Amblyseius cucumeris and swirski [10]. used natural predators from gamma Amblyseius spp.

Table 1. Number of captures by month

No. of table Month Total 4 7 11 13 16 20 24 29 32 51 58 69 74 78 85 89 January 22 15 7 12 5 14 27 6 21 16 17 6 26 19 17 10 240 February 2 0 0 2 2 3 0 3 4 5 2 3 1 3 4 0 34 March 37 4 14 5 7 4 5 2 2 9 3 22 8 4 17 4 147 April 6 3 5 2 10 2 1 0 1 3 2 3 2 3 1 16 60 May 2 10 58 4 6 2 2 3 2 0 6 6 10 3 13 13 138 June 9 18 43 14 6 7 7 5 1 5 3 3 7 3 16 14 161 July 18 17 23 27 32 21 14 13 6 18 8 6 12 7 12 10 244 August 67 88 14 13 12 17 17 10 8 1 23 15 16 24 13 17 355 September 122 61 8 16 10 1 1 1 0 0 132 6 78 41 87 4 568 October 26 8 5 3 4 1 1 0 0 0 28 1 16 9 8 8 118 November 2 0 0 0 0 1 1 0 0 0 0 1 1 1 0 1 8 December 11 21 5 15 10 18 8 15 2 12 4 54 30 30 20 8 263

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In January we observed on the used yellow product that did not affect natural predators, allowing panels a total number of 240 thrips, 44/68/48/33/47 them to be used at the same time as the product in per week a big number of captures. Because of this order to obtain the most effective results. In big number we weekly made 2-3 treatments with September even with all the treatments we still had a Nematoder with different doses and also we placed very big number of catches, 568 individuals, the natural predator, 27 bags/ table. This natural biggest number from all year with 131/114/171/158 predators were used in all the greenhouse, all 81 catches weekly. During these weeks, three different tables not just on the 16. In February we had much treatments were carried out: biological predators, less then in January, meaning that the treatments botanical insecticides, and repeated treatments with were very efficient and at the right time reducing the Nematoder in the largest concentration. These population from 240 individuals to just 34. Even in treatments proved to be very effective by greatly the second month of the year 2017 the capture were reducing the number of individuals in October to 118 decreased significantly to less than 10 individuals per catches. This month also we repeated the Nematoder week we still made one treatment/week with treatments but in smaller doses, and also with Nematoder. From week 10 to 11, 12 the number of Neemazal. captured thrips started to increase from 30 up to 58. Starting from end of November and all In March we had a total number of capture of 147, December we used pheromone traps in parallel with per week 30/44/58/15 individuals. In this month we yellow and blue sticky panels. This method was used made weekly 3 treatments with Nematoder and also for one month, with monitoring once a week. We we placed new bags with natural predators. In April have determined the use of this method at the 50th we had a total number of 60 individuals, also the week due to the occurrence of a larger number of previous treatments proved to be very efficient trips. Thus, at week 50, 94 individuals were captured, reducing the number of population. In this month 58 on blue panels, 51 were observed on pheromone weekly we had less than 10 thrips on the traps, panels and only 7 on control variants; 36 on yellow, because of this small number we dropped the weekly 34 on pheromones, and 2 on control. In view of the treatment with Nematoder, we made just one in each too large number of individuals in this week, 3 second week. treatments with Nematoder in high concentrations In May we observed an increase of the were performed. In week 51, the second week of population number to 138, catching 38/24/43/35 monitoring with the help of blue pheromone traps thrips per week. In this month we repeated weekly the were captured 66 individuals, a fairly large number treatment with Nematoder. From June, July, August considering the treatments performed at week 50. and September the thrips population started to From the total number of 66, 41 trips were observed increase a lot, and we had to supply also the on the blue panels, 30 on pheromone panels and 11 biological treatments with a a biological pesticide on control variants; and 25 yellow panels, of which named Neemazal, a product which prevents 20 are pheromone variants and 5 on control variants. insecticide resistance due to its numerous (> 60) There were made 2 treatments with Nematoder active ingredients, does not contain aflatoxins and in a dose of 1/4 in 500 liters of water, but in order to solvent residues and also doesn’t harm beneficial reduce the number of individuals, we also took 800 insects and predators. ml of Neemazal treatment in 750 liters of water. We From the 25th week, the number of catches also installed additional yellow and simple blue increased considerably from 71 to 161 individuals at panels as well as in combination with pheromones to week 31. In June we had a total number of 161 determine the most effective method of combating, captures, 41/ 71/49 per week. To fight against we the efficiency of sticky panels (yellow and blue) and increased the dose with Nematoder using a whole the efficiency of the pheromones. In the week of packet in 500 l of water, we replaced yellow sticky 52.01.17, 60 individuals were captured, 38 panels with new ones and we doubled the number of individuals on the blue panels, only 3 individuals on natural predators. In July we had a total number of control variants and 35 pheromone variants, 22 244 captured thrips, in week 31 capturing the biggest individuals on the yellow panels, all on pheromone number of 165 individuals. We made weekly 3 variants without any catches on the yellow control treatments with Nematoder, and also we checked the variants. Three treatments with Nematoder ½ were all the tables from this section, we replaced the sticky performed in 500 l of water and were also placed panels and we placed more bags with natural natural predators Amblyseius swirski and cucumeris. predators. In August the number increased more than In the week of 01.02.18, the last week of monitoring in July to 355 thrips, 63/59/123/110 per week. Due to captured 48 individuals, observing a significant the increasing number of individuals, week 34: 123 decrease. Of the total number 35 were observed the catches, week 35: 110 catches we were required to blue variants, 23 on the pheromone panels and 11 on introduce a botanical insecticide called Neemazal, a the control variants, respectively 14 yellow variants,

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10 on the pheromone variants and 4 on the control catches per week, most of them being on the blue variants. The catches were a lot decreased up to 8 pheromonal traps. catches in November and 263 in December. Most of In December from the total number of 263, 165 this catches were on the blue traps, this proving to be were on the blue panels even if just on 7 tables we much more efficient then the yellow ones. In had blue and the rest of 9 were yellow, the number of December we captured 263 individuals, 89/66/60/48 catches on this were much bigger.

January February March April May June July August September October November December

Figure 4. Graph with month catches

4. Conclusions efficient were the blue traps, with or without As a result of the research, we came to the pheromones. Even if they are much more efficient a conclusion that the pheromonal method is very lot of growers are refusing the use of them, because effective, with much better results than the with the help of yellow traps they can catch more pheromone-free control variants. In order to establish kind of pest, white flees, or a larger spectrum of maximum efficiency in pest monitoring, the blue aphids. We can highly recommend the use of blue panels had a much better yield than yellow ones, both traps with and without pheromones in those simple panels used as control and pheromone greenhouses where this very dangerous pest is variants. causing a lot of damages. Pheromone traps are a great pest control tool that is used to help monitor and control insect References infestations. There are pheromone traps for many different types of insects including flies, pantry [1] Allsopp E., 2016, Developing an integrated moths, pantry beetles and cockroaches. Pheromone management system for western flower thrips, traps, when used correctly, are a very effective part Frankliniella occidentalis (Pergande), on deciduous of a pest control program. A pheromone trap usually fruit, using semiochemicals in a push-pull strategy. consists of a small glue trap that is impregnated with sex pheromone or it comes with a small vial of sex [2] Andi N., L.A. Mound, 2016, First record of pheromone that will be placed on the trap. Sex Trialeurodes vaporariorum Westwood pheromones are hormones scents that are usually (&58; Aleyrodidae) severely damaging emitted by the female insect and picked up by the field grown potato crops in South Sulawesi, male as a cue for mating. Male pests are drawn to the Indonesia. Journal of Plant Protection trap for the purpose of mating and are then Research, 56(2), 199-202. caught. This traps proved to be much more efficient then the simple traps, reducing the population fast, [3] Araya J.E., C. Merino, F. Santibanez, L. Sazo, while the simple traps were also catching but in a 2014, Ring spots by feeding of Frankliniella smaller amount. During the research the most occidentalis (Thysanoptera: Thripidae) on white

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