Phthalates esters disrupt demersal fish behavior: Unveiling the brain-gut axis impact
The widespread use of plasticizers like phthalate esters (PAEs) has led to environmental and health concerns. The neurobehavioral toxicity of these compounds in marine environments, particularly regulated by the “brain-gut” axis, remains unclear, especially concerning wild demersal fish of high ecol...
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Elsevier
2025-01-01
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| Series: | Ecotoxicology and Environmental Safety |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S014765132401546X |
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| author | Liuqingqing Liu Xinyao Li Xianxiang Luo Xiao Wang Linjia Liu Zixi Yuan Cuizhu Sun Hao Zheng Elvis Genbo Xu Fengmin Li |
| author_facet | Liuqingqing Liu Xinyao Li Xianxiang Luo Xiao Wang Linjia Liu Zixi Yuan Cuizhu Sun Hao Zheng Elvis Genbo Xu Fengmin Li |
| author_sort | Liuqingqing Liu |
| collection | DOAJ |
| description | The widespread use of plasticizers like phthalate esters (PAEs) has led to environmental and health concerns. The neurobehavioral toxicity of these compounds in marine environments, particularly regulated by the “brain-gut” axis, remains unclear, especially concerning wild demersal fish of high ecological value. Our investigation into the behavioral effects of three common PAEs, i.e., dimethyl phthalate (DMP), di-n-butyl phthalate (DBP), and di(2-ethylhexyl) phthalate (DEHP), and their molecular mechanisms on juvenile Sebastes schlegelii, revealed alarming results from molecular to population levels. After a 20-day foodborne exposure at a low marine environmental concentration (1.0 μg g−1), we observed that all three PAEs significantly increased the thigmotaxis (behavioral tendency to stay close to physical boundaries) and mobility of juvenile fish by 28.2–59.4 % and 23.3–74.5 %, respectively, indicating anxiety-like behavior of fish. DEHP exhibited the most pronounced effects, followed by DBP and DMP. PAEs accumulated in the juvenile fish in the order of brain > liver > gut > muscle, with DEHP showing the highest brain concentrations (23.2 ± 2.98 μg g−1). This accumulation led to oxidative damage, inflammatory responses, and neurodegenerative changes in the optic tectum, resulting in cholinergic system dysfunction. In the gut, PAEs caused inflammatory lesions, disrupted the gut barrier, and altered the gut microbiome, exacerbating the neurotoxicity via “brain-gut” communication. These findings underscore the significant neurobehavioral toxicity of PAEs, emphasizing their critical impact on fish behavior. We also stress the crucial need for further research on fish and other marine species beyond the laboratory scale to fully understand the broader implications of PAE exposure in marine ecosystems and to guide future conservation efforts. |
| format | Article |
| id | doaj-art-dc229f094a384b219d001eca5a4b30d7 |
| institution | Kabale University |
| issn | 0147-6513 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ecotoxicology and Environmental Safety |
| spelling | doaj-art-dc229f094a384b219d001eca5a4b30d72025-01-23T05:25:40ZengElsevierEcotoxicology and Environmental Safety0147-65132025-01-01289117470Phthalates esters disrupt demersal fish behavior: Unveiling the brain-gut axis impactLiuqingqing Liu0Xinyao Li1Xianxiang Luo2Xiao Wang3Linjia Liu4Zixi Yuan5Cuizhu Sun6Hao Zheng7Elvis Genbo Xu8Fengmin Li9Institute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, ChinaInstitute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, ChinaInstitute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, China; Sanya Oceanographic Institution, Ocean University of China, Sanya 57200, China; Corresponding authors at: Institute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, ChinaMarine Agriculture Research Center, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao 266101, ChinaInstitute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, ChinaInstitute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, ChinaInstitute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, ChinaInstitute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, China; Sanya Oceanographic Institution, Ocean University of China, Sanya 57200, China; Corresponding authors at: Institute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, ChinaDepartment of Biology, University of Southern Denmark, 5230 Odense M, DenmarkInstitute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ministry of Education, Ocean University of China, Qingdao 266100, China; Sanya Oceanographic Institution, Ocean University of China, Sanya 57200, ChinaThe widespread use of plasticizers like phthalate esters (PAEs) has led to environmental and health concerns. The neurobehavioral toxicity of these compounds in marine environments, particularly regulated by the “brain-gut” axis, remains unclear, especially concerning wild demersal fish of high ecological value. Our investigation into the behavioral effects of three common PAEs, i.e., dimethyl phthalate (DMP), di-n-butyl phthalate (DBP), and di(2-ethylhexyl) phthalate (DEHP), and their molecular mechanisms on juvenile Sebastes schlegelii, revealed alarming results from molecular to population levels. After a 20-day foodborne exposure at a low marine environmental concentration (1.0 μg g−1), we observed that all three PAEs significantly increased the thigmotaxis (behavioral tendency to stay close to physical boundaries) and mobility of juvenile fish by 28.2–59.4 % and 23.3–74.5 %, respectively, indicating anxiety-like behavior of fish. DEHP exhibited the most pronounced effects, followed by DBP and DMP. PAEs accumulated in the juvenile fish in the order of brain > liver > gut > muscle, with DEHP showing the highest brain concentrations (23.2 ± 2.98 μg g−1). This accumulation led to oxidative damage, inflammatory responses, and neurodegenerative changes in the optic tectum, resulting in cholinergic system dysfunction. In the gut, PAEs caused inflammatory lesions, disrupted the gut barrier, and altered the gut microbiome, exacerbating the neurotoxicity via “brain-gut” communication. These findings underscore the significant neurobehavioral toxicity of PAEs, emphasizing their critical impact on fish behavior. We also stress the crucial need for further research on fish and other marine species beyond the laboratory scale to fully understand the broader implications of PAE exposure in marine ecosystems and to guide future conservation efforts.http://www.sciencedirect.com/science/article/pii/S014765132401546XEndocrine disrupting chemicalsNeurotoxicityBrain-gut axisAnxiety behaviorGut microbiomeBehavioral ecology |
| spellingShingle | Liuqingqing Liu Xinyao Li Xianxiang Luo Xiao Wang Linjia Liu Zixi Yuan Cuizhu Sun Hao Zheng Elvis Genbo Xu Fengmin Li Phthalates esters disrupt demersal fish behavior: Unveiling the brain-gut axis impact Ecotoxicology and Environmental Safety Endocrine disrupting chemicals Neurotoxicity Brain-gut axis Anxiety behavior Gut microbiome Behavioral ecology |
| title | Phthalates esters disrupt demersal fish behavior: Unveiling the brain-gut axis impact |
| title_full | Phthalates esters disrupt demersal fish behavior: Unveiling the brain-gut axis impact |
| title_fullStr | Phthalates esters disrupt demersal fish behavior: Unveiling the brain-gut axis impact |
| title_full_unstemmed | Phthalates esters disrupt demersal fish behavior: Unveiling the brain-gut axis impact |
| title_short | Phthalates esters disrupt demersal fish behavior: Unveiling the brain-gut axis impact |
| title_sort | phthalates esters disrupt demersal fish behavior unveiling the brain gut axis impact |
| topic | Endocrine disrupting chemicals Neurotoxicity Brain-gut axis Anxiety behavior Gut microbiome Behavioral ecology |
| url | http://www.sciencedirect.com/science/article/pii/S014765132401546X |
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