© by PSP Volume 28 ± No. 9/2019 pages 6701-6706 Fresenius Environmental Bulletin

DETERMINING THE CRITERION AND BIOTECHNICAL STRUGGLE METHODS AGAINST FORFICULA AURICULARIA L. (DERMAPTERA: FORFICULIDAE) HARMING IN APRICOT ORCHARDS IN

Mehmet Kaplan*

Department of Plant Protection, Faculty of Agriculture, University, Siirt, Turkey

ABSTRACT mainland of apricot, which is a significant type of fruit that is grown for economic reasons, includes This study was carried out to determine the Iran, Turkistan, Afghanistan, Central Asia and damage and to investigate biotechnical struggle Western China [2]. methods of Forficula auricularia Lin. (Dermaptera: In the world, an annual total of 4,257,241 tons Forficulidae) that damage the apricot orchards of of fresh apricot is produced, while approximately province in 2014-2016. 985,000 tons of this is provided by Turkey. With As a result of the studies, it was determined this degree of production, Turkey is at the first that F. auricularia spent as adult and different SODFHLQWKHZRUOG¶VDSULFRWSURGXFWLRQE\DVKDUHRI nymph periods under the soil, rocks and the shells about 23%. It is followed by Uzbekistan, Italy, Iran of the old trees in the apricot orchards and in the and Pakistan [3]. surrounding areas during the winter. Adults, eggs 7XUNH\LVSURPLQHQWLQWKHZRUOG¶VSURGXction and nymphs of F. auricularia were first found un- of fresh and dried apricots. The reason for this is der rocks beneath the tree bark of old trees and in that the varieties of apricot in Turkey have high various sheltered places in nature between the end potential due to their high-quality and ecological of March and the third week of April. It had been superiorities. The province of Malatya, which is in determined that The density of F. auricularia has the in Turkey, has approx- been increasing since May in the follow-ups of imately 8 million apricot trees, while it matches cardboard traps set up in trees in the apricot or- approximately 68% of the apricot production and chards. 85% of the dried apricot production in the entire It was determined that F. auricularia has been country. Almost all apricot products that are pro- fed on the fruits and formed the highest population duced in the province of Malatya are dried and during the period until harvest from the second exported [3]. week of June when the fruit began to be sweetened There are several pests in apricot orchards that in observations made. Along with that, cardboard directly or indirectly affect quality and yield nega- traps, pit traps and biological insecticide studies tively in terms of the issue of protecting the plants. have been conducted to develop an alternative One of these pests is Earwig causing a significant struggle against pests amount of product and quality loss, feeds on the fruits of these trees and creates harm and is known as Forficula auricularia L. (Dermaptera: Forculi- KEYWORDS: dae)]. Apricot, Forficula auricularia L., Biological criteria The population of the pest in question is in- biotechnical, Turkey creasingly higher in the apricot fields in Malatya, there is no product for protecting plants against this pest, and producers of apricot complain about caus- INTRODUCTION ing decrease in amount of product and quality loss, feeds on the fruits of these trees caused by F. auric- Apricot is a fruit with a very high nutritional ularia. In this context, this study was carried out capacity in addition to being able to be processed with the purpose of, in addition to controlling this into several types of products and having a tasty pest, proposal of some biotechnical precautions to nature. Apricot is a type of fruit belonging to the be taken in controlling weeds in the period of 2014- Prunophora subgenus of the Prunus genus in the 2016. subfamily of Prunoideae in the family of Rosaceae. As a result of this study, alternative control The vast majority of the varieties of apricot that are methods were determined against F. auricularia grown globally belong to the species of Prunus and weeds, and fundamental data were obtained for armeniaca L. (Armeniaca vulgaris Lam.) [1]. The both producers and technical professionals who

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deal with apricot production in both Malatya and pest had sufficient density and was homogenously Turkey in general. distributed. Plant characteristics (cultivation tech- nique, plant size, crown width, inter-row and above-row distance etc.) have been recorded during MATERIALS AND METHODS the trial. The trial has been based on randomized blocks test pattern. The trial has been set with 4 The main material of the study consisted of the repetitions, in a manner to form the characters of apricot orchards in the districts of and the trial, preparation to be tested, sub-dosages and Kale in the province of Malatya, the pest Forficula proof and each parcel contained 3 x 3 = 9 trees. A auricularia L., Azadirachtin, cardboard, pitfall trap trial has been similarly set in proof parcel. with fish oil, insect collection tool and laboratory Three different dosages of Azadirachtin have equipment. been used (500, 400, 300 ml/100 lt water) as bio- insecticide in the study. All components of the trees Determining the Biologic Criteria for Com- have been well sprinkled during the study, and as batting Forficula auricularia L. In this method, this pest is nocturnal, proceedings took place at fortnight and weekly observations have been made evening times. Use of insecticides started once the respectively during the winter months and other amount of individuals inside the trap reached 20 months at the study orchards. During the observa- and fruits started to mature. tions, certain places such as beneath tree shells, With the purpose of establishing the damage plant residues and other similar places have been caused by F. auricularia on fruits at the end of the checked. Their nests have been sought in the soil study, 1.000 fruits have been counted per tree and and shelter traps have been set on five different visually inspected at each parcel during harvest. trees to create a spot for them to hide. This way, the Results have been assessed over the harmed fruit egg laying period, nymph periods and maturing ratios by using Abbott (%) formula and the impacts periods of the pest have been examined to reveal its of the practise have been defined. biology in nature. Statistical Methods Used For Assessment Searching for Opportunities to Counter Purposes. With regards to the analyses during the Forficula auricularia L. a- Use of Carton Shelter statistical assessment of the obtained results, 21.0 Trap and Pitfall Trap Methods. F. auricularia is version of SPSS Statistical Package Program has nocturnal and it looks for shelter in the mornings. been used and One-Way Anova Univariate has been This characteristic was the reason behind develop- applied for LSD and DUNCAN multiple compari- ing the carton shelter trap method [4] F. auricularia son tests hav been applied for the inter-group com- is reported to release a wavy grouping pheromone parisons. [5]. When F. auricularia individuals are removed from the trees thanks to this artificial shelter- grouping pheromone, it will reportedly become RESULTS AND DISCUSSION possible to establish control against it [6]. Carton shelter trap and pitfall trap study has been conduct- The assessments regarding the wintering be- ed in two apricot orchards, one each in Battalgazi haviour of F. auricularia held at the end of this and Kale districts, where 9 trees comprised a parcel. study revealed that it spends the winter during adult In carton shelter tarp, one trap has been set on each and different nymph periods inside the shells of old tree, and in pitfall trap two traps each with a 15 cm trees and underneath rocks, and also within the diameter and containing fish oil have been set on fissures and cracks of soil. [7], reported that the pest both sides of the trunk of a tree. spends winter under fallen leaves, inside the cracks Traps have been set at a time when apricots in soil, [8. 9.10] reported it spends the winter as a started to get their taste and the pest began to be adult, [11] reported it spends the winter as a mature seen commonly (20-30 adults/traps in average) and inside the cracks in tree branches and trunks, un- they have been replaced with a new one in every derneath shells and rocks and other shelters such as three days until harvest. Traps have been set in wall cracks. orchards on 16 June 2015 and kept until the harvest Adult individuals of F. auricularia have been on 2 July, and during 2016, they have been set on spotted for the first time on 09 April 2015 and 29 21 June 2016 and used until harvesting on 12 July. Mart 2016 in various protected places in non- processed areas such as pastures outside the apricot b-Bioinsecticide trial Against Forficula au- orchards along with mature female individuals and ricularia L. Suitable intervals have been used for eggs (each set containing 35-45 eggs) on 16 April planting during the study and the selected orchards 2015 and 05 April 2016, and nymphs have been were the same age, yielding products normally and spotted in nature on 21 April 2015 and 14 April harmed by F. auricularia a year ago. Before the 2016. Female individuals of F. auricularia have practise, attention has been paid to see whether the been observed to lay their eggs 3-5 cm below soil

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surface and hatching nymphs emerged from here. vember 2016 and afterwards the matures and Individuals of F. auricularia have been sighted for nymphs went into seclusion for wintering. [20], the last time on 29 April 2015 and 02 May 2016. reported that F. auricularia reached a high popula- [12] Reported that F. auricularia lays its eggs in 2 tion level in July but it kept diminishing in the fol- sets, the first laid eggs hatch on mid-April and lowing months and by September around half of the nymphs start to appear on surface during late April population left the orchard. It has also been reported and early May; [13], the pest is laying its eggs into that Adult individuals of F. auricularia in early 5 cm-deep cracks close to the soil surface in sets October and moved into the soil but a small amount consisting of 30-60 eggs; [8.9], F. auricularia of individuals stayed on trees until early November. spends the winter as a adult, eggs are stored to- With regards to the corrugated carton traps set wards the end of winter and hatch during May and for developing alternative countering methods adult in August, each nymph period took place in against F. auricularia; the fruit ratio in the apricot 12 days when average temperature in laboratory orchard trees harmed by F. auricularia in Battalga- conditions was 15-20 °C; [14], females laid 50 to zi and Kale districts in 2015 was 10.62% and 90 eggs and laid them about 5-8 mm deep from the 8.75%, proof was 43.75% and 36.50%, efficiency soil surface; [10], mature females have been ob- was 76.75% and 80.33%, and in 2016 harmed fruit tained through sampling from April to October, ratio was 10.00% and 11.87%, proof was 40.00% while male individuals have been obtained from and 46.25% and efficiency was 80.19% and 72.87% August to October, matures were able to mate after (Table 1). [21], reported that F. auricularia can be wintering and lay their eggs once or twice until the found in orchards and can be caught if a single-wall end of May; [11], F. auricularia is the sole incubat- fibreboard is attached on a tree branch during au- ing insect that looks after the new-born and a fe- tumn; [22], reported that carton shelter traps can be male lays 20-80 eggs (2-3 eggs at a time); [15], effective if replaced on a daily basis or twice a reported nymphs hatching from the eggs laid by week when combating F. auricularia; [16], report- female of F. auricularia during mid-April started ed that they have used carton traps because F. au- climbing to the soil surface by late April and early ricularia is nocturnal and gathers in dark and shel- May, and adult by late June or early July; [16], tered places during daytime and also that they re- reported adult females lay around 30-50 eggs in placed the traps every 2-3 days. their underground nests. In terms of pitfall trap method, the fruit ratio The first adults and nymphs of the pest in na- in the apricot orchard trees harmed by F. auricular- ture have been observed in apricot orchards in Ma- ia in Battalgazi and Kale districts in 2015 was latya province on 05 May 2015 and 11 May 2016, 36.25% and 40.00%, proof was 45.00% and adult density kept increasing in the following 46.25% and efficiency was 18.53% and 15.78%. weeks, it started feeding-off the apricots when they and in 2016 fruit ratio harmed by F. auricularia started gaining taste (16 June 2015 and 21 June was 38.12% and 35.00% respectively, proof was 2016), reached a great density during the period 47.75% and 38.5% and efficiency was 17.29% and leading to harvest (02 July 2015 and 12 July 2016) 17.65% (Table 2). [15], Conducted a study in and caused damage in apricot fruit at a ratio ranging Southern Washington state in USA surveying F. between 33.9% and 47.75%.; [17], reported that F. auricularia in pitfall traps set in bushland. The auricularia can cause harm in apricot and nectarine months of April and May witnessed the highest orchards to a degree ranging between 10% and amount of non-adult individuals caught in pitfall 40%; [18], reported the harm caused by F. auricu- traps while mid-July was the time when the highest laria in organic peach orchards is over 20%, harm amount of adult individuals have been caught. [16], occurs a few days before harvest as the pest opens Conducted a study on the pest in USA, monitoring wide holes inside the ripe fruits and lead to signifi- its population and catching with traps, and used cant economic harm in peach. [19], reported that F. carton traps as well as pitfall traps containing oil auricularia density increases in traps when ap- fish for population monitoring during summer proaching to harvest during June and July and the months and replaced the traps in every 2-3 days. harm caused in apricots is between 5% and 14%. The ratio of harmed fruits during the bio- Adult density kept diminishing following har- insecticide (Azadirachtin 500-400-300 ml/ 100 lt. vest and the last adults in apricot orchards have water) trials in apricot orchards in Battalgazi and been spotted during October (28 October 2014, 12 Kale districts in 2015 was 14.85% and 6.40% re- October 2015 and 04 October 2016). The observa- spectively, proof ratio was 40.62% and 33.90% and tions made led to the conclusion that the adults efficiency was 79.75% and 81.11%, and in 2016 moving from apricot orchards into non-processed harmed fruit ratio was 7.81% and 7.03% respective- areas, such as pastures, outside the apricot orchards ly, proof was 46.25% and 41.10% while efficiency started mating during the month of October and the was 82.75% and 80.75% (Table 3, 4). adults and first eggs were spotted on 28 October Looking at the Variance Analysis Tables pro- 2015 and 11 November 2016, then the first nymphs vided in table 3 and 4, there is a meaningful differ- were spotted on 17 November 2015 and 23 No- ence of 95% reliability between the averages of 300

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ml and 400 ml, 300 ml-500 ml dosages, but to the outcomes in both locations and in both years. Vari- contrary, there is no meaningful difference between ance analysis yielded a statistical difference of 0.01 the 400 ml and 500 ml dosages. As such, the con- between practises but no differences have been clusion reached was that 400 ml dosage of the in- observed between locations. secticide can be recommended against adult indi- 500ml and 400ml dosages of Azadirachtin and viduals F. auricularia in apricot orchards. [23], also corrugated carton traps yielded the greatest reported that Neem extract (Azadirachtin) reduces efficiency against F. auricularia in apricot orchards nymph population of F. auricularia on peach trees and the fruits on trees have not been harmed much. by 70%. [16], Conducted a study on pest- But in contrast, 300 ml dosage and pitfall trap not management in peach orchards and recommended only yielded the lowest effect but the harm on fruits Azadirachtin when combating earwig. was at a higher level. Therefore, when combating The efficiency at 400 and 500 ml dosages in adult individuals of F. auricularia in apricot or- both districts was statistically placed within the chards, use of 400 ml dosage of Azadirachtin or same group while 300 ml dosage has been placed in corrugated carton traps, one of the biotechnical a different group. In terms of effect (%) during the methods, can be recommended. trials, the pesticides and traps yielded the same

TABLE 1 (%) effects of cardboard trap trial against the adults of Forficula auricularia Lin. (Dermaptera:Forficulidae) in 2015 and 2016 in the apricot orchards of Number of Medicated (a) Loss Rate in Fruits (%) Efficiency (%) Date examined Control (b) fruit Battalgazi Kale Battalgazi Kale a 10.62 8.75 76.75 80.33 02.07.2015 1000 b 43.75 36.50 a 10.00 11.87 80.19 72.87 12.07.2016 1000 b 40.00 46.25

TABLE 2 (%) effects of pitfall trap trial against the adults of Forficula auricularia Lin. (Dermaptera:Forficulidae) in 2015 and 2016 in the apricot orchards of Malatya Province Number of Medicated (a) Loss Rate in Fruits (%) Efficiency (%) Date examined Control (b) fruit Battalgazi Kale Battalgazi Kale a 36.25 40.00 18.53 15.78 02.07.2015 1000 b 45.00 46.25 a 38.12 35.00 17.29 17.65 12.07.2016 1000 b 47.75 38.50

TABLE 3 Statistical analysis of Azadirachtin against the adults of Forficula auricularia Lin. (Dermaptera:Forficulidae)in the apricot orchards of Malatya Province in 2015 The name of the drug Loss Rate in Fruits (%) Efficiency (%) Dosage/100lt water Battalgazi Kale Battalgazi Kale 500 8.12 6.40 79.75 a 81.11 a 400 8.90 7.97 77.50 a 76.50 a Azadirachtin 300 14.85 12.65 63.46 b 62.67 b Control 40.62 33.90 - -

TABLE 4 Statistical analysis of Azadirachtin against the adults of Forficula auricularia Lin. (Dermaptera:Forficulidae)in the apricot orchards of Malatya Province in 2016 The name of the drug Loss Rate in Fruits (%) Efficiency (%) Dosage/100lt water Battalgazi Kale Battalgazi Kale 500 7.81 7.03 82.75 a 80.75 a 400 9.37 8.59 79.18 a 79.46 a Azadirachtin 300 12.81 12.50 72.64 b 69.45 b Control 46.25 41.10 - -

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CONCLUSION [7] Chant, D.A., Mcleod, J.H. (1952) Effects of Certain Climatic Factors on The Daily Abun- In conclusion, it has been observed that F. au- dance of The European Earwig, Forficula au- ricularia is becoming populated in orchards, feed- ricularia L. (Dermaptera: Forficulidae), in ing off-apricots as they start to get tasty and is Vancouver, British Columbia. Canadian En- harming them until harvest time. The density of tom. 84, 174-180. pests and the amount of harm done in these areas [8] Lamb, R.J., Wellington, W.G., (1974) Tech- varies per year. niques for Studying the Behavior and Ecology Use of chemical pesticides needs to be avoid- of The European Earwig, Forficula auricularia ed at the beginning to maintain environmental (Dermaptera: Forficulidae). Canadian Ento- health and natural balance and biotechnical and mologist. 106, 881-888. cultural methods need to be employed instead. [9] Lamb, R.J., Wellington, W.G. (1975) Life Apricot is a product that is both consumed domesti- History and Population Characteristics of The cally and is being exported abroad therefore it is European Earwig, Forficula auricularia (Der- necessary to prioritize biotechnical methods and maptera: Forficulidae), at Vancouver, British cultural measures to ensure no residues are left on Columbia. Canadian Entomologist. 107, 819- the product. 824. [10] Kocarek, P. (1998) Life Cycles and Habitat Associations of Three Earwig (Dermaptera) ACKNOWLEDGEMENTS Species in Lowland Forest and Its Surround- ings. Biologia, Bratislava. 53(2), 205-211. [11] Öztürk, N., Ulusoy, R. (2010) Earwig is harm- We are thankful to the General Directorate of ful in Malatya Apricot. Plant Protection Agricultural Research and Policies that supported Directorate Bereket (2010-5) liflet. this research. [12] Crumb, S.E., Eide, P.M., Bonn, A.E. (1941) This study was presented as a summary in the 2nd International Mediterranean Science and Engi- The European Earwig. USDA Technical Bulle- neering Congress October 25-27, 2017. tin 766.76p. [13] BuxtoN, J.H., Madge, D.S. (1974) Artificial Incubation of Eggs of the Common Earwig, Forficula auricularia (L.). Entomologist's REFERENCES Monthly Magazine. 110, 55-57. [14] Weems, H.V., Skelley, Paul, E. (1989) Europe- [1] Bailey, C.H. and Hough, L.F. (1975) Apricots. an earwig, Forficula auricularia Linnaeus In: Janick, J. and Moore, J.N. (Eds.) Advances (Dermaptera: Forficulidae). Entomology Circu- Fruit Breeding. Purdue University Press. West lar, No: 318. Fla. Dept. Agric and Consumer of Lafayette, Indiana, USA. 367-383. Plant Industry. [2] (UFLúOL 6   $SULFRW &XOWXUH LQ 7XUNH\ [15] Zack, R.S., Strenge, D., Landolt, P.J., and Scientific Research and Essay. 4(8), 715-719. Looney, C. (2010) European Earwig, Forficula (In Turkish). auricularia L. (Dermaptera: Forficulidae), at [3] Anonymous. (2017) Static Database of FAO The Hanford Reach National Monument, (Food and Agriculture Organization of the Washington State. Western North American United Nations).http://www.fao.org/faostat/QC Naturalist. 70(4), 441±445. (Accessed date: 04.01.2019. [16] Alston, D.G. and Tebeau, A., (2011) European [4] Lamb, R.J. (1975) Effects of Dispersion, Trav- Earwig (Forficula auricularia). Published by el, and Environmental Heterogeneity on Popu- Utah State University Extension and Utah Plant lations of The Earwig Forficula auricularia L. Pest Diagnostic Laboratory. ENT-145-11. Can. J. Zool. 53, 1855-1867. [17] Santini, L., Caroli, L., (1992) Informatore- [5] Walker, K.A., Jones, T.H., Fell, R.D. (1993) Fitopatologico. 42(5), 35-38, 11 ref. Pheromonal Basis of Aggregation in European [18] Zimmerman, R. (2000) Population and Control Earwig, Forficula auricularia L. (Dermaptera: Study of the European Earwig, Forficula au- Forficulidae). J. Chem. Ecol. 19(9), 2029-2038. ricularia L., in Western Colorado Peach Or- [6] Burnip G.M., Daly, J.M., Hacket J.K., Suck- chards. Research Scientist, W. Colo. Research ling, D.M. (2002) European Earwig Phenology Center-Rogers Mesa. 10p. and Effect of Understorey Management on [19] $\D]7g]JHQøKaplan, M. (2009) Preva- Population Estimation. New Zealand Plant Pro- lence, Population Changing and Damage Ratio tection. 55, 390-395. of Forficula auricularia (Linnaeus, 1758) (Dermaptera: Forficulidae ¶ in Apricot Or- chards of Malatya. Proceedings of The Third Plant Protection Congress of Turkey, Van.

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[20] Gobin, B., Marien, A., Davis S., Leirs, H. (2006) Enhancing Earwig Populations in Bel- gian Orchards. Comm. Appl. Biol. Sci, Ghent University. 71(2b), 269-273. [21] Joseph, L.T. (2000) The European Earwig, Forficula auricularia. Feedback Online: From The Association for the Study of Animal Be- haviour. [22] Jacobs, S., (2009) European earwigs. Pennsyl- vania State University Entomological Notes NP-4, http://ento.psu.edu/extension/factsheets /pdf/european Earwigs. [23] Sauphor, B., Lenfant, C., Sureau F. (1995) Effects of a neem seed extract (Azadirachta in- dica A. Juss) on the development of the Der- maptera, Forficula auricularia L. Journal of Applied Entomology. 119(1-5), 215-219.

Received: 12.02.2019 Accepted: 20.06.2019

CORRESPONDING AUTHOR

Mehmet Kaplan University of Siirt, Faculty of Agriculture Department of Plant Protection, 56100 Siirt ± Turkey e-mail: [email protected]

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