Ariane Guimarães, Abraão Tiago Batista Guimarães, Rafaela Ribeiro de Brito, Alex Rodrigues Gomes, Ítalo Nascimento Freitas, Aline Sueli de Lima Rodrigues, Omar Cruz Santiago, Thiarlen Marinho da Luz, Letícia Paiva de Matos, Raíssa Ferreira de Oliveira, Guilherme Malafaia
{"title":"Necroecological Trophic Transfer of Microplastics: Insights into the Ecotoxicity of Petroleum-Derived and Biodegradable Polymers.","authors":"Ariane Guimarães, Abraão Tiago Batista Guimarães, Rafaela Ribeiro de Brito, Alex Rodrigues Gomes, Ítalo Nascimento Freitas, Aline Sueli de Lima Rodrigues, Omar Cruz Santiago, Thiarlen Marinho da Luz, Letícia Paiva de Matos, Raíssa Ferreira de Oliveira, Guilherme Malafaia","doi":"10.1007/s00244-025-01120-1","DOIUrl":null,"url":null,"abstract":"<p><p>Although the toxicity of petroleum-derived microplastics (MPs) has been widely investigated, the impact of biomicroplastics (BioMPs) remains controversial, and the necroecological trophic transfer of both is still poorly understood. Our study reveals that biomicroplastics may pose ecotoxicological risks comparable to or greater than those of petroleum-derived plastics, a finding that should raise concern. We aimed to evaluate the possible translocation of polystyrene (PS) and polylactic acid (PLA) MPs from mice to the necrophagous fly Synthesiomyia nudiseta and their potential effects on the larval stage. Mice were inoculated intraperitoneally with different doses of MPs [9 (I) and 90 mg/kg (II)] and subjected to the decomposition process (for ten days), allowing colonization by larvae. Our results confirmed the translocation of MPs from mice to S. nudiseta larvae, resulting in a greater accumulation of PLA-MPs compared to PS-MPs. We observed that exposure to MPs significantly influenced biomass accumulation, with larvae from the PS-I and PLA-I groups showing increased biomass. In contrast, those from the PLA-II group exhibited lower biomass. AChE activity was modulated in a concentration-dependent manner, with an increase observed in larvae exposed to PLA-MPs, indicating a potential neurotoxic effect. In addition, there was an increased production of reactive oxygen species (ROS), especially in the groups exposed to higher concentrations of MPs, without a proportional response of antioxidant enzymes, suggesting a redox imbalance and oxidative stress. The elevated serotonin levels and reduced dopamine observed in larvae exposed to MPs indicate a possible redirection of energy resources and changes related to a metabolic adaptation to the stress imposed by MPs. Principal component analysis (PCA) showed that PC1 was strongly influenced by biomarkers such as trypsin, chymotrypsin, AChE, ROS, and dopamine activity, highlighting that PLA-MPs (at the highest concentration) induced more pronounced toxic effects than PS-MPs. This finding was corroborated by discriminant analysis, which revealed a clear separation between the experimental groups, and by multiple regression analysis, which confirmed a strong relationship between MP concentration and larval biomarker responses, indicating that the type and concentration of MPs explained approximately 65% of the variation in the biomarkers evaluated. In conclusion, our study demonstrates for the first time the necroecological trophic translocation of MPs between vertebrates and invertebrates, highlighting the potential risks of biomicroplastics.</p>","PeriodicalId":8377,"journal":{"name":"Archives of Environmental Contamination and Toxicology","volume":" ","pages":""},"PeriodicalIF":3.7000,"publicationDate":"2025-02-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Archives of Environmental Contamination and Toxicology","FirstCategoryId":"93","ListUrlMain":"https://doi.org/10.1007/s00244-025-01120-1","RegionNum":4,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"ENVIRONMENTAL SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Although the toxicity of petroleum-derived microplastics (MPs) has been widely investigated, the impact of biomicroplastics (BioMPs) remains controversial, and the necroecological trophic transfer of both is still poorly understood. Our study reveals that biomicroplastics may pose ecotoxicological risks comparable to or greater than those of petroleum-derived plastics, a finding that should raise concern. We aimed to evaluate the possible translocation of polystyrene (PS) and polylactic acid (PLA) MPs from mice to the necrophagous fly Synthesiomyia nudiseta and their potential effects on the larval stage. Mice were inoculated intraperitoneally with different doses of MPs [9 (I) and 90 mg/kg (II)] and subjected to the decomposition process (for ten days), allowing colonization by larvae. Our results confirmed the translocation of MPs from mice to S. nudiseta larvae, resulting in a greater accumulation of PLA-MPs compared to PS-MPs. We observed that exposure to MPs significantly influenced biomass accumulation, with larvae from the PS-I and PLA-I groups showing increased biomass. In contrast, those from the PLA-II group exhibited lower biomass. AChE activity was modulated in a concentration-dependent manner, with an increase observed in larvae exposed to PLA-MPs, indicating a potential neurotoxic effect. In addition, there was an increased production of reactive oxygen species (ROS), especially in the groups exposed to higher concentrations of MPs, without a proportional response of antioxidant enzymes, suggesting a redox imbalance and oxidative stress. The elevated serotonin levels and reduced dopamine observed in larvae exposed to MPs indicate a possible redirection of energy resources and changes related to a metabolic adaptation to the stress imposed by MPs. Principal component analysis (PCA) showed that PC1 was strongly influenced by biomarkers such as trypsin, chymotrypsin, AChE, ROS, and dopamine activity, highlighting that PLA-MPs (at the highest concentration) induced more pronounced toxic effects than PS-MPs. This finding was corroborated by discriminant analysis, which revealed a clear separation between the experimental groups, and by multiple regression analysis, which confirmed a strong relationship between MP concentration and larval biomarker responses, indicating that the type and concentration of MPs explained approximately 65% of the variation in the biomarkers evaluated. In conclusion, our study demonstrates for the first time the necroecological trophic translocation of MPs between vertebrates and invertebrates, highlighting the potential risks of biomicroplastics.
期刊介绍:
Archives of Environmental Contamination and Toxicology provides a place for the publication of timely, detailed, and definitive scientific studies pertaining to the source, transport, fate and / or effects of contaminants in the environment. The journal will consider submissions dealing with new analytical and toxicological techniques that advance our understanding of the source, transport, fate and / or effects of contaminants in the environment. AECT will now consider mini-reviews (where length including references is less than 5,000 words), which highlight case studies, a geographic topic of interest, or a timely subject of debate. AECT will also consider Special Issues on subjects of broad interest. The journal strongly encourages authors to ensure that their submission places a strong emphasis on ecosystem processes; submissions limited to technical aspects of such areas as toxicity testing for single chemicals, wastewater effluent characterization, human occupation exposure, or agricultural phytotoxicity are unlikely to be considered.