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Translocation of clothianidin to guttation fluid and its potential impact on honey bee, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae)

Yıl 2021, Cilt: 45 Sayı: 4, 511 - 522, 15.12.2021

Melis Yalçın , İlknur Kapiz Mustafa Kösoğlu , Onur Koca , Nalan Turgut , Erkan Topal , Perihan Binnur Kurt Karakuş , Levent Atatanır , Serhan Mermer , Merve Özkaleli Akçetin , Jens Pistorius Cafer Turgut

https://doi.org/10.16970/entoted.1017479
Cited By: 3

Öz

Honey bees, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae) forage water from guttation fluid so transported neonicotinoid insecticides in guttation fluid poses a risk to the bees. The first aim of this study was to determine the toxicity and risk of clothianidin to honey bees. In addition, the changes of clothianidin residue in the guttation fluid of maize plants in Turkey were determined in 2018 and 2019. Also, the toxicity of guttation fluid collected from the maize plants to bees was determined in ecotoxicological tests. The acute oral LD50 of clothianidin to honey bees in the first 24 h was 1.80 ng bee-1 and residue analysis demonstrated that honey bees were exposed to clothianidin concentration in guttation fluid ranging from 0.02 to 6.0 mg L-1 with mortality ranging between 80 and 100%. As the measured concentration of clothianidin in guttation fluid can lead to the mortality of honey bees, present study indicates that clothianidin, and possibly related pesticides in treated maize seed poses a risk to honey bees. Future studies are needed to determine the scale and distribution of this risk in Turkey.

Anahtar Kelimeler

Clothianidin exposure risk guttation honey bees residue

Destekleyen Kurum

Scientific and Technological Research Council of Turkey (TÜBİTAK), Project No: TOVAG 118O522 for 2019 field studies and Aydın Adnan Menderes University Research Funds, Project No: ZRF-18016 for 2018

Proje Numarası

Scientific and Technological Research Council of Turkey (TÜBİTAK), Project No: TOVAG 118O522; Aydın Adnan Menderes University Research Funds, Project No: ZRF-18016

Teşekkür

This work was supported by the Scientific and Technological Research Council of Turkey (TÜBİTAK), Project No: TOVAG 118O522 for 2019 field studies and Aydın Adnan Menderes University Research Funds, Project No: ZRF-18016 for 2018 field studies.

Kaynakça

  • Abdelkader, F. B., İ. Çakmak, S. S. Çakmak, Z. Nur, E. İncebıyık, A. Aktar & H. Erdost, 2021. Toxicity assessment of chronic exposure to common insecticides and bee medications on colony development and drones sperm parameters. Ecotoxicology, 30 (5): 806-817.
  • Akyol, E. & O. Kaftanoğlu, 2001. Colony characteristics and the performance of Caucasian (Apis mellifera caucasica) and Mugla (Apis mellifera anatoliaca) bees and their reciprocal crosses. Journal of Apicultural Research, 40 (3): 11-15.
  • Alkassab, A. T. & W. H. Kirchner, 2016. Impacts of chronic sublethal exposure to clothianidin on winter honeybees. Ecotoxicology, 25 (5): 1000.
  • Anastassiades, M., S. J. Lehotay, D. Stajnbaher & F. J. Schenck, 2003. Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. Journal of AOAC International, 86 (2): 412-431.
  • Anonymous, 2021. Republic of Turkey Ministry of Food, Agriculture and Livestock, Department of Plant Protection Products. (Web page: https://bku.tarimorman.gov.tr) (Data accessed: September, 2021).
  • Brandt, A., A. Gorenflo, R. Siede, M. Meixner & R. Büchler, 2016. The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). Journal of Insect Physiology, 86: 40-47.
  • Brandt, A., K. Grikscheit, R. Siede, R. Grosse, M. D. Meixner & R. Büchler, 2017. Immunosuppression in honeybee queens by the neonicotinoids thiacloprid and clothianidin. Scientific Reports, 7 (4673): 1-12.
  • Çakmak, İ., 2018. Effects of thiamethoxam on the behavior of foraging honey bees with artificial flower choices. Uludağ Arıcılık Dergisi, 18 (1): 2-13.
  • Çil, G. İ., S. D. Korkmaz, G. Ozansoy & Ö. Küplülü, 2020. Türkiye’deki bal örneklerinde neonicotinoid varlığının LC-MS/Q-TOF yöntemi ile tespiti. Mehmet Akif Ersoy University Journal of Health Sciences Institute, 8 (1): 11-17. (In Turkish with abstract in English).
  • Codling, G., Y. A. Naggar, J. P. Giesy & A. J. Robertson, 2016. Concentrations of neonicotinoid insecticides in honey, pollen and honey bees (Apis mellifera L.) in central Saskatchewan, Canada. Chemosphere, 144: 2321-2328.
  • Cutler, G. C. & C. D. Scott-Dupree, 2007. Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. Ecotoxicology, 100 (3): 765-772.
  • Cutler, G., C. D. Scott-Dupree, M. Sultan, A. D. McFarlane & L. Brewer, 2014. A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. PeerJ, 2 (e652): 1-23.
  • Di Prisco, G., V. Cavaliere, D. Annoscia, P. Varricchio, E. Caprio, F. Nazzi, G. Gargiulo & F. Pennacchio, 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. PNAS Proceedings of the National Academy of Sciences of the United States of America, 110 (46): 18466-18471.
  • EFSA, 2013. Conclusion on the peer review of the pesticide risk assessment for bees for the active substance thiamethoxam. EFSA Journal, 11 (1): 3067.
  • Flores, J. M., V. Gamiz, S. Gil-Lebrero, I. Rodriguez, F. J. Navas, A. I. Garcia-Valcarcel, V. Cutillas, A. R. Fernandez-Alba & M. D. Hernando, 2021. A three-year large-scale study on the risk of honey bee colony exposure to blooming sunflowers grown from seeds treated with thiamethoxam and clothianidin neonicotinoids. Chemosphere, 262 (127735): 1-9.
  • Frommberger, M., J. Pistorius, I. Joachimsmeier & D. Schenke, 2011. ʺGuttation and the risk for honey bee colonies (Apis mellifera L.): a worst case semi-field scenario in maize with special consideration of impact on bee brood and brood development, 71-75ʺ. 11th International Symposium of the ICP-BR Bee Protection Group (2-4 November 2011, Wageningen, The Netherlands), Julius-Kühn-Archiv, 437 pp.
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  • Girolami, V., M. Marzaro, L. Vivan, L. Mazzon, M. Greatti, C. Giorio, D. Marton & A. Tapparo, 2012. Fatal powdering of bees in flight with particules of neonicotinoids seed coating and humidity implication. Journal of Applied Entomology, 136 (1-2):17-26.
  • Huff Hartz, K. E., T. M. Edwards & M. J. Lydy, 2017. Fate and transport of furrow-applied granular tefluthrin and seed-coated clothianidin insecticides: Comparison of field-scale observations and model estimates. Ecotoxicology, 26 (7): 876-888.
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Clothianidinin gutasyon sıvısında taşınımı ve bal arısı, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae) üzerindeki etkisinin belirlenmesi

Yıl 2021, Cilt: 45 Sayı: 4, 511 - 522, 15.12.2021

Melis Yalçın , İlknur Kapiz Mustafa Kösoğlu , Onur Koca , Nalan Turgut , Erkan Topal , Perihan Binnur Kurt Karakuş , Levent Atatanır , Serhan Mermer , Merve Özkaleli Akçetin , Jens Pistorius Cafer Turgut

https://doi.org/10.16970/entoted.1017479
Cited By: 3

Öz

Öz
Bal arılarının, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae) gutasyon sıvısından su ihtiyacını karşılaması sırasında gutasyon sıvısında tohum ilacı olarak kullanılan neonicotinoid insektisitlerin taşınması arılarda risk yaratmaktadır. Bu çalışmanın ilk amacı clothianidinin arılara toksisitesi ve riskinin belirlenmesidir. Bunun yanında 2018 ve 2019 yıllarında Türkiye’de mısır bitkisindeki gutasyon sıvısında clothianidin kalıntısının değişimleri belirlenmiştir. Ayrıca mısır bitkisinden toplanan gutasyon sıvılarının arılara toksisitesinde yapılan ekotoksikolojik testlerde tespit edilmiştir. Clothianidinin ilk 24 saatteki bal arılarına olan toksisitesi incelendiğinde ortalama akut oral LD50 değeri 1.80 ng arı-1 olarak saptanmıştır. Bununla birlikte kalıntı analizleri sonucunda bal arılarının gutasyon sıvısında 0.02 mg L-1 ile 6 mg L-1 arasında değişen clothianidin konsantrasyonuna maruz kaldığı tespit edilmiş olup bal arılarının ölüm oranının %80 ile %100 arasında değiştiği gözlenmiştir. Gutasyon sıvısında ölçülen clothianidin konsantrasyonu bal arılarının ölümüne yol açabileceğinden, bu çalışma, mısır tohumlarına uygulanan clothianidin ve benzer grupta olan pestisitlerin, bal arıları için risk oluşturduğunu göstermektedir. Bu riskin Türkiye’deki miktarını ve dağılımını belirlemek için gelecekte yapılacak çalışmalara ihtiyaç vardır.

Anahtar Kelimeler

Clothianidin maruziyet riski gutasyon bal arıları kalıntı

Proje Numarası

Scientific and Technological Research Council of Turkey (TÜBİTAK), Project No: TOVAG 118O522; Aydın Adnan Menderes University Research Funds, Project No: ZRF-18016

Kaynakça

  • Abdelkader, F. B., İ. Çakmak, S. S. Çakmak, Z. Nur, E. İncebıyık, A. Aktar & H. Erdost, 2021. Toxicity assessment of chronic exposure to common insecticides and bee medications on colony development and drones sperm parameters. Ecotoxicology, 30 (5): 806-817.
  • Akyol, E. & O. Kaftanoğlu, 2001. Colony characteristics and the performance of Caucasian (Apis mellifera caucasica) and Mugla (Apis mellifera anatoliaca) bees and their reciprocal crosses. Journal of Apicultural Research, 40 (3): 11-15.
  • Alkassab, A. T. & W. H. Kirchner, 2016. Impacts of chronic sublethal exposure to clothianidin on winter honeybees. Ecotoxicology, 25 (5): 1000.
  • Anastassiades, M., S. J. Lehotay, D. Stajnbaher & F. J. Schenck, 2003. Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. Journal of AOAC International, 86 (2): 412-431.
  • Anonymous, 2021. Republic of Turkey Ministry of Food, Agriculture and Livestock, Department of Plant Protection Products. (Web page: https://bku.tarimorman.gov.tr) (Data accessed: September, 2021).
  • Brandt, A., A. Gorenflo, R. Siede, M. Meixner & R. Büchler, 2016. The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). Journal of Insect Physiology, 86: 40-47.
  • Brandt, A., K. Grikscheit, R. Siede, R. Grosse, M. D. Meixner & R. Büchler, 2017. Immunosuppression in honeybee queens by the neonicotinoids thiacloprid and clothianidin. Scientific Reports, 7 (4673): 1-12.
  • Çakmak, İ., 2018. Effects of thiamethoxam on the behavior of foraging honey bees with artificial flower choices. Uludağ Arıcılık Dergisi, 18 (1): 2-13.
  • Çil, G. İ., S. D. Korkmaz, G. Ozansoy & Ö. Küplülü, 2020. Türkiye’deki bal örneklerinde neonicotinoid varlığının LC-MS/Q-TOF yöntemi ile tespiti. Mehmet Akif Ersoy University Journal of Health Sciences Institute, 8 (1): 11-17. (In Turkish with abstract in English).
  • Codling, G., Y. A. Naggar, J. P. Giesy & A. J. Robertson, 2016. Concentrations of neonicotinoid insecticides in honey, pollen and honey bees (Apis mellifera L.) in central Saskatchewan, Canada. Chemosphere, 144: 2321-2328.
  • Cutler, G. C. & C. D. Scott-Dupree, 2007. Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. Ecotoxicology, 100 (3): 765-772.
  • Cutler, G., C. D. Scott-Dupree, M. Sultan, A. D. McFarlane & L. Brewer, 2014. A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. PeerJ, 2 (e652): 1-23.
  • Di Prisco, G., V. Cavaliere, D. Annoscia, P. Varricchio, E. Caprio, F. Nazzi, G. Gargiulo & F. Pennacchio, 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. PNAS Proceedings of the National Academy of Sciences of the United States of America, 110 (46): 18466-18471.
  • EFSA, 2013. Conclusion on the peer review of the pesticide risk assessment for bees for the active substance thiamethoxam. EFSA Journal, 11 (1): 3067.
  • Flores, J. M., V. Gamiz, S. Gil-Lebrero, I. Rodriguez, F. J. Navas, A. I. Garcia-Valcarcel, V. Cutillas, A. R. Fernandez-Alba & M. D. Hernando, 2021. A three-year large-scale study on the risk of honey bee colony exposure to blooming sunflowers grown from seeds treated with thiamethoxam and clothianidin neonicotinoids. Chemosphere, 262 (127735): 1-9.
  • Frommberger, M., J. Pistorius, I. Joachimsmeier & D. Schenke, 2011. ʺGuttation and the risk for honey bee colonies (Apis mellifera L.): a worst case semi-field scenario in maize with special consideration of impact on bee brood and brood development, 71-75ʺ. 11th International Symposium of the ICP-BR Bee Protection Group (2-4 November 2011, Wageningen, The Netherlands), Julius-Kühn-Archiv, 437 pp.
  • Girolami, V., L. Mazzon, A. Squartini, N. Mori, M. Marzaro, A. D. Bernardo, M. Greatti, C. Giorino & A. Tapparo, 2009. Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: a novel way of intoxication for bees. Journal of Economic Entomology, 102 (5): 1808-1815.
  • Girolami, V., M. Marzaro, L. Vivan, L. Mazzon, M. Greatti, C. Giorio, D. Marton & A. Tapparo, 2012. Fatal powdering of bees in flight with particules of neonicotinoids seed coating and humidity implication. Journal of Applied Entomology, 136 (1-2):17-26.
  • Huff Hartz, K. E., T. M. Edwards & M. J. Lydy, 2017. Fate and transport of furrow-applied granular tefluthrin and seed-coated clothianidin insecticides: Comparison of field-scale observations and model estimates. Ecotoxicology, 26 (7): 876-888.
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  • Moncharmont, F. X. D., A. Decourtye, C. Hennequet-Hantier, O. Pons & M. Pham-Delegue, 2003. Statistical analysis of honeybee survival after chronic exposure to insecticides. Environmental Toxicology and Chemistry, 22 (12): 3088-3094.
  • Mörtl, M., A. Vehovszky, S. Klatyik, E. Takacs, J. Györi & A. Szekacs, 2020. Neonicotinoids: spreading, translocation and aquatic toxicity. International Journal of Environmental Research and Public Health, 17 (6): 1-24.
  • Nauen, R., U. Ebbinghaus-Kintscher & R. Schmuck, 2001. Toxicity and nicotinic acetylcholine receptor interaction of imidacloprid and its metabolites in Apis mellifera (Hymenoptera: Apidae). Pest Management Science, 57 (7): 577-586.
  • Nikolakis, A., J. Keppler, M. Miles & R. Schoening, 2014. ʺNeonicotinoid seed treatment products – Occurrence and relevance of guttation for honeybee colonies, 160-167ʺ. 12th International Symposium of the ICP-PR Bee Protection Group (15-17 September 2014, Ghent, Belgium), 450 pp.
  • OECD, 1998. ʺAcute Oral Toxicity Test No: 213ʺ. In: OECD Guidelines for Testing of Chemicals Honeybees. Organization for Economic Cooperation and Development, Paris, 9 pp.
  • Palmer, M. J., C. Moffat, N. Saranzewa, J. Harvey, G. A. Wright & C. N. Connolly, 2013. Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nature Communications, 4 (1634): 1-8.
  • Pihlström, T., 2011. ʺAnalytical Method Validation and Performance Criteria, 9-15ʺ. In: Method Validation and Quality Control Procedures for Pesticide Residues Analysis in Food and Feed (Eds. M. Anastassiades, A. Andersson, P. Cuhra, A. Kok, J. Durcanska, M. E. Poulsen, A. R. Fernandez-Alba, M. Gamon, R. Lippold, O. Malato, P. Medina, P. Pelosi, P. Ravio, S. Reynolds, A. Valverde & W. Zachariae). National Food Administration Uppsala, Sweeden, 41 pp.
  • Pistorius, J., T. Brobyn, P. Campbell, R. Forster, J. A. Lortsch, F. Marolleau, C. Maus, J. Lückmann, H. Suzuki, K. Wallner & R. Becker, 2012 ʺAssessment of risks to honey bees posed by guttation, 199-208ʺ. 11th International Symposium of the ICP-BR Bee Protection Group (2-4 November 2011, Wageningen, The Netherlands), Julius-Kühn-Archiv, 437 pp.
  • Reetz, J. E., W. Schulz, W. Seitz, M. Spiteller, S. Zühlke, W. Armbruster & K. Wallner, 2016. Uptake of neonicotinoid insecticides by water-foraging Honey Bees (Hymenoptera: Apidae) through guttation fuid of winter oilseed Rape. Journal of Economic Entomology, 109 (1): 31-40.
  • Reetz, J. E., S. Zühlke, M. Spiteller & K. Wallner, 2011. Neonicotinoid insecticides translocated in guttated droplets of seed-treated maize and wheat: A threat to honeybees? Apidologie, 42 (5): 596-606.
  • Rundlöf, M., G. K. S. Andersson, R. Bommarco, I. Fries, V. Hederström, L. Herbertsson, O. Jonsson, B. K. Klatt, T. R. Pedersen, J. Yourstone & H. G. Smith, 2015. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature, 521 (7551): 77-80.
  • Samson-Robert, O., G. Labrie, M. Chagnon & V. Fournier, 2017. Planting of neonicotinoid-coated corn raises honey bee mortality and sets back colony development. PeerJ, 5 (e3670): 1-24.
  • Sanchez-Hernandez, L., D. Hernández-Domínguez, M. T. Martin, M. J. Nozal, M. Higes & J. L. B. Yagüe, 2016. Residues of neonicotinoids and their metabolites in honey and pollen from sunflower and maize seed dressing crops. Journal of Chromatography A, 1428: 220-227.
  • Sandrock, C., L. G. Tanadini, J. S. Pettis, J. C. Biesmeijer, S. G. Potts & P. Neumann, 2014. Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agricultural and Forest Entomology, 16 (2): 119-128.
  • Schenke, D., I. P. Wirtz, S. Lorenz, J. Pistorius & U. Heimbach, 2018. Two-year field data on neonicotinoid concentrations in guttation drops of seed treated maize (Zea mays). Data in Brief, 21: 299-306.
  • Schmolke A., B. Kearns & B. O'neil, 2018. Plant guttation water as a potential route for pesticide exposure in honey bees: a review of recent literature. Apidologie, 49 (5): 637-646.
  • Schmuck, R. & J. Keppler, 2003. Clothianidin–Ecotoxicological profile and risk assessment. Pflanzenschutz-Nachrichten Bayer 56: 26-58.
  • Schmuck, R., R. Schöning, A. Stork & O. Schramel, 2001. Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Management Science, 57 (3): 225-238.
  • Schneider, C. W., J. Tautz, B. Grünewald & S. Fuchs, 2012. RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. Plos One, 7 (1): 1-9.
  • Scholer, J. & V. Krischik, 2014. Chronic exposure of imidacloprid and clothianidin reduce queen survival, foraging, and nectar storing in colonies of bombus impatiens. Plos One, 9 (3): 1-14.
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  • Wirtz, I. P., M. H. Jakli, D. Schenke, E. Ladewig, B. Marlander, U. Heimbach & J. Pistorius, 2018. Investigations on neonicotinoids in guttation fluid of seed treated sugar beet: Frequency, residue levels and discussion of the potential risk to honey bees. Crop Protection, 105: 28-34.
  • Woodcock, B. A., J. M. Bullock, R. F. Shore, M. S. Heard, M. G. Pereira, J. Redhead, L. Ridding, H. Dean, D. Sleep, P. Henrys, J. Peyton, S. Hulmes, L. Hulmes, M. Sarospataki, C. Saure, M. Edwards, E. Genersch, S. Knabe & R. F. Pywell, 2017. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science, 356 (6345): 1393-1395.
  • WSDA, 2010. Pollinator protection requirements for Section 18 Emergency Exemptions and Section 24 (c) special local need registration in Washington State. (Web page: https: //agr.wa.gov/departments/pesticides) (Date accessed: November 2021).
Toplam 65 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Bölüm Makaleler
Yazarlar

Melis Yalçın 0000-0002-9122-7133

İlknur Kapiz Bu kişi benim 0000-0001-8045-1837

Mustafa Kösoğlu 0000-0001-6616-089X

Onur Koca 0000-0002-0753-0077

Nalan Turgut 0000-0001-5099-5024

Erkan Topal 0000-0002-1398-4390

Perihan Binnur Kurt Karakuş 0000-0001-6737-3475

Levent Atatanır 0000-0001-5638-6676

Serhan Mermer 0000-0003-2949-6372

Merve Özkaleli Akçetin 0000-0001-5593-7966

Jens Pistorius Bu kişi benim 0000-0002-7707-1216

Cafer Turgut 0000-0002-6450-5361

Proje Numarası Scientific and Technological Research Council of Turkey (TÜBİTAK), Project No: TOVAG 118O522; Aydın Adnan Menderes University Research Funds, Project No: ZRF-18016
Erken Görünüm Tarihi 17 Kasım 2021
Yayımlanma Tarihi 15 Aralık 2021
Gönderilme Tarihi 5 Kasım 2021
Kabul Tarihi 20 Ocak 2022
Yayımlandığı Sayı Yıl 2021 Cilt: 45 Sayı: 4

Kaynak Göster

APA Yalçın, M., Kapiz, İ., Kösoğlu, M., Koca, O., vd. (2021). Translocation of clothianidin to guttation fluid and its potential impact on honey bee, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae). Turkish Journal of Entomology, 45(4), 511-522. https://doi.org/10.16970/entoted.1017479
AMA Yalçın M, Kapiz İ, Kösoğlu M, Koca O, Turgut N, Topal E, Karakuş PBK, Atatanır L, Mermer S, Özkaleli Akçetin M, Pistorius J, Turgut C. Translocation of clothianidin to guttation fluid and its potential impact on honey bee, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae). TED. Aralık 2021;45(4):511-522. doi:10.16970/entoted.1017479
Chicago Yalçın, Melis, İlknur Kapiz, Mustafa Kösoğlu, Onur Koca, Nalan Turgut, Erkan Topal, Perihan Binnur Kurt Karakuş, Levent Atatanır, Serhan Mermer, Merve Özkaleli Akçetin, Jens Pistorius, ve Cafer Turgut. “Translocation of Clothianidin to Guttation Fluid and Its Potential Impact on Honey Bee, Apis Mellifera Anatoliaca Maa, 1953 (Hymenoptera: Apidae)”. Turkish Journal of Entomology 45, sy. 4 (Aralık 2021): 511-22. https://doi.org/10.16970/entoted.1017479.
EndNote Yalçın M, Kapiz İ, Kösoğlu M, Koca O, Turgut N, Topal E, Karakuş PBK, Atatanır L, Mermer S, Özkaleli Akçetin M, Pistorius J, Turgut C (01 Aralık 2021) Translocation of clothianidin to guttation fluid and its potential impact on honey bee, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae). Turkish Journal of Entomology 45 4 511–522.
IEEE M. Yalçın, “Translocation of clothianidin to guttation fluid and its potential impact on honey bee, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae)”, TED, c. 45, sy. 4, ss. 511–522, 2021, doi: 10.16970/entoted.1017479.
ISNAD Yalçın, Melis vd. “Translocation of Clothianidin to Guttation Fluid and Its Potential Impact on Honey Bee, Apis Mellifera Anatoliaca Maa, 1953 (Hymenoptera: Apidae)”. Turkish Journal of Entomology 45/4 (Aralık 2021), 511-522. https://doi.org/10.16970/entoted.1017479.
JAMA Yalçın M, Kapiz İ, Kösoğlu M, Koca O, Turgut N, Topal E, Karakuş PBK, Atatanır L, Mermer S, Özkaleli Akçetin M, Pistorius J, Turgut C. Translocation of clothianidin to guttation fluid and its potential impact on honey bee, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae). TED. 2021;45:511–522.
MLA Yalçın, Melis vd. “Translocation of Clothianidin to Guttation Fluid and Its Potential Impact on Honey Bee, Apis Mellifera Anatoliaca Maa, 1953 (Hymenoptera: Apidae)”. Turkish Journal of Entomology, c. 45, sy. 4, 2021, ss. 511-22, doi:10.16970/entoted.1017479.
Vancouver Yalçın M, Kapiz İ, Kösoğlu M, Koca O, Turgut N, Topal E, Karakuş PBK, Atatanır L, Mermer S, Özkaleli Akçetin M, Pistorius J, Turgut C. Translocation of clothianidin to guttation fluid and its potential impact on honey bee, Apis mellifera anatoliaca Maa, 1953 (Hymenoptera: Apidae). TED. 2021;45(4):511-22.

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