Alterations Induced by Nano-Polystyrene Administration in Biological Parameters of Host-Endoparasitoids (Galleria mellonella and Pimpla turionellae) and Host Hemocyte Counts

Abstract

Plastic pollution is one of the biggest threats to the environment and human health. Micro and nanoplastics are encountered in many areas of our daily lives and may accumulate in organisms, causing reduced life span, genotoxicity, and altered metabolism. Plastic pollution around the environment may lead to reductions in insect biodiversity and populations. It may also lead to the collapse of food webs and ecosystems of organisms that feed on them in the food chain. Therefore, the effects of nano-polystyrene (PSs) on the life cycle, biological characteristics, total hemocyte count (THCs) of the host, and hemocyte types of the model organism Galleria mellonella and its endoparasitoid Pimpla turionellae were investigated. Nano-PSs were produced according to the single emulsion solvent evaporation method and larval feeds were prepared with solutions of different concentrations. These diets were given to the larvae until they developed. The developmental time of the host-larvae fed with nano-PS-containing diets and the parasitoids that emerged using the pupae of these larvae as hosts were shortened. While the host adult weight and size increased, the weight of the parasitoid decreased. Dose-dependent decreases in THCs were observed. Prohemocyte, plasmatocyte, oenocytoid, and spherulocyte counts decreased, while granulocyte counts increased. Furthermore, the changes in the biology of the host exposed to nano-PSs indirectly affected the endoparasitoids. In addition, this study emphasizes that nanoplastic toxicity in honey-bees is generally ignored and that the consumption of bee products may pose potential hazards to human health. This reveals the crucial role of taking necessary precautions in beekeeping.

Keywords

• Cellular immunity
• greater wax moth
• life cycle
• nano-plastic
• parasitoid wasp

Supporting Institution

This study was supported by the Kocaeli University Scientific Research Projects Coordination Department under Grant Number: FYL-2021-2345.

Project Number

FYL-2021-2345

Ethical Statement

Ethics committee approval is not required for this study.

Thanks

This study is the MSc thesis of Tuğba Nur ELLİBEŞ GÖKKAYA. We are grateful to Ezgi ÇOĞAL for her experimental help. Hemocytes data were presented as a poster at the 7th International Marmara Science Congress-IMASCON in 2021. This study was supported by the Kocaeli University Scientific Research Projects Coordination Department under Grant Number: FYL-2021-2345.

Nano-Polistiren Uygulamasının Konak-Endoparazitoitlerin (Galleria mellonella ve Pimpla turionellae) Biyolojik Parametrelerinde ve Konak Hemosit Sayılarında Oluşturduğu Değişiklikler

Abstract

Plastik kirliliği çevre ve insan sağlığı açısından en büyük tehditlerden biridir. Mikro ve nanoplastikler, günlük yaşamımızın birçok alanında karşımıza çıkmaktadır ve organizmalarda birikerek yaşam süresinin azalmasına, genotoksisiteye ve metabolizmanın değişmesine neden olabilmektedir. Çevredeki nanoplastik kontaminasyonu, böcek biyoçeşitliliğindeki ve popülasyonlarındaki azalmalara neden olabilir. Aynı zamanda besin zincirinde onlarla beslenen canlıların besin ağlarının ve ekosistemlerin çökmesine yol açabilir. Bu nedenle nano-polistiren (PS)’lerin model organizma Galleria mellonella ve endoparazitoiti Pimpla turionellae’nın yaşam döngüsüne, biyolojik özelliklerine, konağın toplam hemosit sayısına (THS) ve hemosit tiplerine etkileri incelendi. Nano-PS’ler tekli emülsiyon çözücü buharlaştırma yöntemine göre üretildi ve farklı konsantrasyonlarda solüsyonları ile larval besinler hazırlandı. Bu besinler, larvalara gelişinceye kadar verildi. Nano-PS içeren besinlerle beslenen konak larvaların ve bu larvaların pupalarını konak olarak kullanarak ortaya çıkan parazitoitlerin gelişim süreleri kısaldı. Konak ergin ağırlığı ve boyutları artarken, parazitoitin ağırlığı azaldı. THS’de doza bağlı azalmalar görüldü. Prohemosit, plazmatosit, önositoid ve sferülosit sayısının azaldığı, granülosit sayısının ise arttığı görüldü. Ayrıca nano-PS’lerle beslenen konağın biyolojisindeki değişiklikler, endoparazitoitleri dolaylı olarak etkiledi. Öte yandan bu çalışma ile bal arılarında nanoplastik toksisitesinin genellikle göz ardı edildiği ve arı ürünlerinin tüketilmesinin insan sağlığı için potansiyel tehlikeler yaratabileceği vurgulanmaktadır. Bu durum, arıcılıkta gerekli önlemlerin alınmasının önemini ortaya koymaktadır.

Keywords

• Hücresel bağışıklık
• büyük balmumu güvesi
• yaşam döngüsü
• nano-plastik

Supporting Institution

Bu çalışma, Kocaeli Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Daire Başkanlığı tarafından FYL-2021-2345 numaralı proje kapsamında desteklenmiştir.

Project Number

FYL-2021-2345

Ethical Statement

Bu çalışma için etik kurul iznine gerek yoktur.

Thanks

Bu çalışma Tuğba Nur ELLİBEŞ GÖKKAYA'nın Yüksek Lisans tezidir. Deneysel yardımları için Ezgi ÇOĞAL'a minnettarız. Hemosit verileri 2021 yılında 7. Uluslararası Marmara Bilim Kongresi-IMASCON'da poster olarak sunuldu. Bu çalışma Kocaeli Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Dairesi Başkanlığı tarafından proje Numarası: FYL-2021-2345 kapsamında desteklenmiştir.

References

1. Aloisi, M., Grifoni, D., Zarivi, O., Colafarina, S., Morciano, P., & Poma, A.M.G. (2024). Plastic Fly: What Drosophila melanogaster Can Tell Us about the Biological Effects and the Carcinogenic Potential of Nanopolystyrene. International Journal of Molecular Sciences, 25(14), 7965. https://doi.org/10.3390/ijms25147965
2. Altuntaş, H., Kılıç, A.Y., Uçkan, F., & Ergin, E. (2012). Effects of Gibberellic Acid on Hemocytes of Galleria mellonella L. (Lepidoptera: Pyralidae). Environmental Entomology, 41(3), 688-696. https://doi.org/10.1603/en11307
3. Awet, T.T., Kohl, Y., Meier, F., Straskraba, S., Grün, A.L., Ruf, T., … & Emmerling, C. (2018). Effects of polystyrene nanoparticles on the microbiota and functional diversity of enzymes in soil. Environmental Sciences Europe, 30(1), 11. https://doi.org/10.1186/s12302-018-0140-6
4. Bronskill, J. (1961). A cage to simplify the rearing of the greater wax moth, Galleria mellonella (Pyralidae). Journal of the Lepidopterists' Society, 15(2), 102-104.
5. Calderone, N.W. (2012). Insect Pollinated Crops, Insect Pollinators and US Agriculture: Trend Analysis of Aggregate Data for the Period 1992–2009. PLOS ONE, 7(5), e37235. https://doi.org/10.1371/journal.pone.0037235
6. Demirtürk, Z., Uçkan, F., & Mert, S. (2024). Interactions of alumina and polystyrene nanoparticles with the innate immune system of Galleria mellonella. Drug and Chemical Toxicology, 47(5), 483-495. https://doi.org/10.1080/01480545.2023.2217484
7. Deng, Y., Jiang, X., Zhao, H., Yang, S., Gao, J., Wu, Y., … & Hou, C. (2021). Microplastic Polystyrene Ingestion Promotes the Susceptibility of Honeybee to Viral Infection. Environmental Science & Technology, 55(17), 11680-11692. https://doi.org/10.1021/acs.est.1c01619
8. Dolar, A., Drobne, D., Dolenec, M., Marinšek, M., & Jemec Kokalj, A. (2022). Time-dependent immune response in Porcellio scaber following exposure to microplastics and natural particles. Science of the Total Environment, 818, 151816. https://doi.org/10.1016/j.scitotenv.2021.151816

9. Dolar, A., Selonen, S., van Gestel, C.A.M., Perc, V., Drobne, D., & Jemec Kokalj, A. (2021). Microplastics, chlorpyrifos and their mixtures modulate immune processes in the terrestrial crustacean Porcellio scaber. Science of The Total Environment, 772, 144900. https://doi.org/10.1016/j.scitotenv.2020.144900
10. El Kholy, S., & Al Naggar, Y. (2023). Exposure to polystyrene microplastic beads causes sex-specific toxic effects in the model insect Drosophila melanogaster. Scientific Reports, 13(1), 204. https://doi.org/10.1038/s41598-022-27284-7
11. Gounari, S., Goras, G., & Thrasyvoulou, A. (2024). Dibrachys cavus, a promising parasitoid in the biological control of the greater wax moth (Galleria mellonella). Journal of Apicultural Research, 63(2), 323-328. https://doi.org/10.1080/00218839.2021.2008707
12. Guimarães, A.T.B., de Lima Rodrigues, A.S., Pereira, P.S., Silva, F.G., & Malafaia, G. (2021). Toxicity of polystyrene nanoplastics in dragonfly larvae: An insight on how these pollutants can affect bentonic macroinvertebrates. Science of The Total Environment, 752, 141936. https://doi.org/10.1016/j.scitotenv.2020.141936
13. Hu, D., Shen, M., Zhang, Y., Li, H., & Zeng, G. (2019). Microplastics and nanoplastics: would they affect global biodiversity change? Environmental Science and Pollution Research, 26(19), 19997-20002. https://doi.org/10.1007/s11356-019-05414-5
14. Hu, M., & Palić, D. (2020). Micro- and nano-plastics activation of oxidative and inflammatory adverse outcome pathways. Redox Biology, 37, 101620. https://doi.org/10.1016/j.redox.2020.101620
15. Kalman, J., Muñiz-González, A.B., García, M.Á., & Martínez-Guitarte, J.L. (2023). Chironomus riparius molecular response to polystyrene primary microplastics. Science of the Total Environment, 868, 161540. https://doi.org/10.1016/j.scitotenv.2023.161540
16. Kholy, S.E., & Naggar, Y.A. (2022). Polystyrene Microplastic Beads Caused Cellular Alterations in midgut cells and Sex-Specific Toxic Effects on Survival, Starvation Resistance, and Excretion of the Model Insect Drosophila melanogaster. Research Square. https://doi.org/10.21203/rs.3.rs-1977878/v1
17. Kim, S.W., & An, Y.J. (2019). Soil microplastics inhibit the movement of springtail species. Environment International, 126, 699-706. https://doi.org/10.1016/j.envint.2019.02.067
18. Kögel, T., Bjorøy, Ø., Toto, B., Bienfait, A.M., & Sanden, M. (2020). Micro- and nanoplastic toxicity on aquatic life: Determining factors. Science of The Total Environment, 709, 136050. https://doi.org/10.1016/j.scitotenv.2019.136050
19. Long, M., Paul-Pont, I., Hégaret, H., Moriceau, B., Lambert, C., … & Soudant, P. (2017). Interactions between polystyrene microplastics and marine phytoplankton lead to species-specific hetero-aggregation. Environmental Pollution, 228, 454-463. https://doi.org/10.1016/j.envpol.2017.05.047
20. Martin-Folgar, R., Sabroso, C., Cañas-Portilla, A.I., Torres-Ruíz, M., González-Caballero, M.C., Dorado, H., … & Morales, M. (2024). DNA damage and molecular level effects induced by polystyrene (PS) nanoplastics (NPs) after Chironomus riparius (Diptera) larvae. Chemosphere, 346, 140552. https://doi.org/10.1016/j.chemosphere.2023.140552
21. Muhammad, A., Zhang, N., He, J., Shen, X., Zhu, X., Xiao, J., … & Shao, Y. (2024). Multiomics analysis reveals the molecular basis for increased body weight in silkworms (Bombyx mori) exposed to environmental concentrations of polystyrene micro- and nanoplastics. Journal of Advanced Research, 57, 43-57. https://doi.org/10.1016/j.jare.2023.09.010
22. Muhammad, A., Zhou, X., He, J., Zhang, N., Shen, X., Sun, C., … & Shao, Y. (2021). Toxic effects of acute exposure to polystyrene microplastics and nanoplastics on the model insect, silkworm Bombyx mori. Environmental Pollution, 285, 117255. https://doi.org/10.1016/j.envpol.2021.117255
23. Murphy, F., Ewins, C., Carbonnier, F., & Quinn, B. (2016). Wastewater Treatment Works (WwTW) as a Source of Microplastics in the Aquatic Environment. Environmental Science & Technology, 50(11), 5800-5808. https://doi.org/10.1021/acs.est.5b05416
24. Oliveira, M., Almeida, M., & Miguel, I. (2019). A micro(nano)plastic boomerang tale: A never ending story? TrAC Trends in Analytical Chemistry, 112, 196-200. https://doi.org/10.1016/j.trac.2019.01.005
25. Outhwaite, C.L., McCann, P., & Newbold, T. (2022). Agriculture and climate change are reshaping insect biodiversity worldwide. Nature, 605(7908), 97-102. https://doi.org/10.1038/s41586-022-04644-x
26. Parenti, C.C., Binelli, A., Caccia, S., Della Torre, C., Magni, S., Pirovano, G., & Casartelli, M. (2020). Ingestion and effects of polystyrene nanoparticles in the silkworm Bombyx mori. Chemosphere, 257, 127203. https://doi.org/10.1016/j.chemosphere.2020.127203
27. Peng, B.Y., Xu, Y., Zhou, X., Wu, W.M., & Zhang, Y. (2024). Generation and Fate of Nanoplastics in the Intestine of Plastic-Degrading Insect (Tenebrio molitor Larvae) during Polystyrene Microplastic Biodegradation. Environmental Science & Technology, 58(23), 10368-10377. https://doi.org/10.1021/acs.est.4c01130
28. Rothen-Rutishauser, B., Bogdanovich, M., Harter, R., Milosevic, A., & Petri-Fink, A. (2021). Use of nanoparticles in food industry: current legislation, health risk discussions and public perception with a focus on Switzerland. Toxicological & Environmental Chemistry, 103(4), 423-437. https://doi.org/10.1080/02772248.2021.1957471
29. Sak, O., Uçkan, F., & Ergin, E. (2006). Effects of cypermethrin on total body weight, glycogen, protein, and lipid contents of Pimpla turionellae (L.) (Hymenoptera: Ichneumonidae). Belgian Journal of Zoology, 136(2006), 53-58.
30. Shafiq ur, R. (2009). Evaluation of malonaldialdehyde as an index of chlorpyriphos insecticide exposure in Apis mellifora: Ameliorating role of melatonin and α-tocopherol against oxidative stress. Toxicological & Environmental Chemistry, 91(6), 1135-1148. https://doi.org/10.1080/02772240802542617
31. Shen, J., Liang, B., & Jin, H. (2023). The impact of microplastics on insect physiology and the indication of hormesis. TrAC Trends in Analytical Chemistry, 165, 117130. https://doi.org/10.1016/j.trac.2023.117130
32. Toussaint, B., Raffael, B., Angers-Loustau, A., Gilliland, D., Kestens, V., Petrillo, M., … & Van den Eede, G. (2019). Review of micro- and nanoplastic contamination in the food chain. Food Additives & Contaminants, Part A, 36(5), 639-673. https://doi.org/10.1080/19440049.2019.1583381
33. Tu, Q., Deng, J., Di, M., Lin, X., Chen, Z., Li, B., … & Zhang, Y. (2023). Reproductive toxicity of polystyrene nanoplastics in Drosophila melanogaster under multi-generational exposure. Chemosphere, 330, 138724. https://doi.org/10.1016/j.chemosphere.2023.138724
34. Uçkan, F., Öztürk, Z., Altuntaş, H., & Ergin, E. (2011). Effects of Gibberellic Acid (GA3) on Biological Parameters and Hemolymph Metabolites of the Pupal Endoparasitoid Pimpla turionellae (Hymenoptera: Ichneumonidae) and its Host Galleria mellonella (Lepidoptera: Pyralidae). Journal of the Entomological Research Society, 13(3), 1-14.
35. Uçkan, F., & Sak, O. (2010). Cytotoxic effect of cypermethrin on Pimpla turionellae (Hymenoptera: Ichneumonidae) larval hemocytes. https://doi.org/10.5053/ekoloji.2010.753
36. Urbisz, A.Z., Małota, K., Chajec, Ł., & Sawadro, M.K. (2024). Size-dependent and sex-specific negative effects of micro- and nano-sized polystyrene particles in the terrestrial invertebrate model Drosophila melanogaster. Micron, 176, 103560. https://doi.org/10.1016/j.micron.2023.103560
37. Voget, M. (1989). Bees and beeproducts as biological indicators of environmental contamination: An economical alternative way of monitoring pollutants. Toxicological & Environmental Chemistry, 20-21(1), 199-202. https://doi.org/10.1080/02772248909357376
38. Wang, J., Coffin, S., Sun, C., Schlenk, D., & Gan, J. (2019). Negligible effects of microplastics on animal fitness and HOC bioaccumulation in earthworm Eisenia fetida in soil. Environmental Pollution, 249, 776-784. https://doi.org/10.1016/j.envpol.2019.03.102
39. Wang, K., Li, J., Zhao, L., Mu, X., Wang, C., Wang, M., … & Wu, L. (2021). Gut microbiota protects honey bees (Apis mellifera L.) against polystyrene microplastics exposure risks. Journal of Hazardous Materials, 402, 123828. https://doi.org/10.1016/j.jhazmat.2020.123828
40. Wang, W., Ge, J., Yu, X., & Li, H. (2020). Environmental fate and impacts of microplastics in soil ecosystems: Progress and perspective. Science of The Total Environment, 708, 134841. https://doi.org/10.1016/j.scitotenv.2019.134841
41. Wang, Z.J., Zhang, Y.H., Gao, R.Y., Jia, H.B., Liu, X.J., Hu, Y.W., … & Zhang, J.P. (2023). Polystyrene Nanoparticle Uptake and Deposition in Silkworm and Influence on Growth. Sustainability, 15(9), 7090. https://doi.org/10.3390/su15097090
42. Zhang, J., Ma, C., Xia, X., Li, Y., Lin, X., Zhang, Y., & Yang, Z. (2023). Differentially Charged Nanoplastics Induce Distinct Effects on the Growth and Gut of Benthic Insects (Chironomus kiinensis) via Charge-Specific Accumulation and Perturbation of the Gut Microbiota. Environmental Science & Technology, 57(30), 11218-11230. https://doi.org/10.1021/acs.est.3c02144