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Temperature-Dependent Biochemical Alterations in Oreochromis niloticus exposed to Pendimethalin and Fluometuron

Year 2025, Volume: 46 Issue: 2, 250 - 256, 30.06.2025

Derya Kocamaz , Mine Beyazaslan , Aşkın Barış Kaya

https://doi.org/10.17776/csj.1630407

Abstract

Pesticides contamination and global warming are significant environmental challenges that threaten aquatic ecosystems. Aquatic organisms are often exposed to pesticide mixtures rather than individual compounds, leading to complex toxicological interactions that may enhance adverse effects. Additionally, temperature increase due to climate change can influence pesticide persistence and toxicity. This study aimed to investigate the combined biochemical effects of pendimethalin and fluometuron mixtures under different temperature conditions in the blood of Oreochromis niloticus. Fish were exposed to environmentally relevant low (0.1 ppb) and high concentrations (1 ppb) of herbicide mixtures for 96 hours at 220C and 280C. Results demonstrated significant interactions between pesticide concentration and temperature for all measured parameters. Cortisol level increased at 220C in both pesticide-exposed groups compared to control, while it decreased at 280C. Estradiol and testosterone levels were reduced 280C in both exposure concentrations. Thyroid hormones (triiodothyronine (T3) and thyroxine (T4)) were reduced in the high concentration group at both temperatures. Alanine aminotransferase (ALT) and aspartate aminotransferase (AST) enzyme activities were decreased across both pesticide concentrations at both temperatures, except in the low concentration group at 280C. Ion levels were also reduced in the high pesticide concentration at 280C. Principal component analysis (PCA) confirmed that the most pronounced biochemical alterations were observed in the high concentration group at 280C, reflecting the synergistic effect of both stressors. These findings suggest that elevated temperature exacerbates the toxic effect of pesticide mixtures, emphasizing the need to examine interactive stressors to better predict the impacts of climate change on non-target organisms

Keywords

Aquatic toxicology Biochemical biomarkers Fish Global warming Pesticide mixtures

References

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  • [2] Noyes P.D., Lema S.C., Forecasting the impacts of chemical pollution and climate change interactions on the health of wildlife, Current Zoology, 61(4) (2015) 669–689.
  • [3] Marchand A., Haddad S., Simultaneous exposures to heat and chemicals and the impact on toxicokinetic and biomonitoring, Current Opinion in Toxicology, 4 (2017) 22–27.
  • [4] Jacquin L., Gandar A., Aguirre-Smith M., Perrault A., Le Hénaff M., De Jong L., Paris-Palacios S., Laffaille P., Jean S., High temperature aggravates the effects of pesticides in goldfish, Ecotoxicology and Environmental Safety, 172 (2019) 255–263.
  • [5] Choudhury P.P., Saha S., Dynamics of pesticides under changing climatic scenario, Environmental Monitoring and Assessment, 192(S1) (2021).
  • [6] Philippe C., Thore E.S.J., Verbesselt S., Gregoir A.F., Brendonck L., Pinceel T., Combined effects of global warming and chlorpyrifos exposure on the annual fish Nothobranchius furzeri, Ecotoxicology and Environmental Safety, 248 (2022) 114290.
  • [7] Luks A.-K., Zegarski T., Nowak K.M., Miltner A., Kästner M., Matthies M., Schmidt B., Schäffer A., Fate of Pendimethalin in Soil and Characterization of Non-Extractable Residues (Ner), Science of the Total Environment, 753 (2021).
  • [8] Vighi M., Matthies M., Solomon K.R., Critical assessment of pendimethalin in terms of persistence, bioaccumulation, toxicity, and potential for long-range transport, J. Toxicol. Environ. Health Part B, 20(1) (2016) 1–21.
  • [9] European Food Safety Authority, Peer review of the pesticide risk assessment of the active substance pendimethalin, EFSA J., (2016).
  • [10] Herrero-Hernandez E., Simon-Egea A.B., Sanchez-Martin M.J., Rodriguez-Cruz M.S., Andrades M.S., Monitoring and environmental risk assessment of pesticide residues and some of their degradation products in natural waters of the Spanish vineyard region included in the Denomination of Origin Jumilla, Environmental Pollution, 264 (2020) 114666.
  • [11] Asman W.A., Jorgensen A., Bossi R., Vejrup K.V., Mogensen B.B., Glasius M., Wet deposition of pesticides and nitrophenols at two sites in Denmark: measurements and contributions from regional sources, Chemosphere, 59(7) (2005) 1023–1031.
  • [12] Barba-Brioso C., Fernandez-Caliani J.C., Miras A., Cornejo J., Galan E., Multi-source water pollution in a highly anthropized wetland system associated with the estuary of Huelva (SW Spain), Marine Pollution Bulletin, 60(8) (2010) 1259–1269.
  • [13] Udarbe Zamora E., Fluometuron, Encyclopedia of Toxicology, 340–342 (2005).
  • [14] Gikas G.D., Vryzas Z., Koshis Z., Experiments on fluometuron removal from simulated agricultural wastewater in porous media filters, Environ. Process., 9(1) (2021).
  • [15] Coupe R.H., Welch H.L., Pell A.B., Thurman E.M., Herbicide and degradate flux in the Yazoo River Basin, Int. J. Environ. Anal. Chem., 85 (2005) 1127–1140 [16] U.S. E.P.A., Chemical Information Fact Sheet Number 88: Fluometuron, Office of Pesticides and Toxic Substances, Washington, DC (1985).
  • [16] de Almeida M.D., Pereira T.S.B., Batlouni S.R., Boscolo C.N.P., de Almeida E.A., Estrogenic and anti-androgenic effects of the herbicide tebuthiuron in male Nile tilapia (Oreochromis niloticus), Aquatic Toxicology, 194 (2018) 86–93
  • [17] Maharaj S., El Ahmadie N., Rheingold S., El Chehouri J., Yang L., Souders C.L., Martyniuk C.J., Sub-lethal toxicity assessment of the phenylurea herbicide linuron in developing zebrafish (Danio rerio) embryo/larvae, Neurotoxicology Teratology, 81 (2020) 106917.
  • [18] Bojarski B.L., Swadźba-Karbowy M., Makulska J., Jakubiak M., Pawlak K., Tombarkiewicz B., Witeska M., Effects of herbicides pendimethalin and ethofumesate on common carp (Cyprinus carpio) erythrocyte morphology, Folia Biologica, 66(3) (2018) 143–149.
  • [19] Gupta P., Verma S.K., Impacts of herbicide pendimethalin on sex steroid level, plasma vitellogenin concentration and aromatase activity in teleost Clarias batrachus (Linnaeus), Environmental Toxicology and Pharmacology, 75 (2020) 103324.
  • [20] Herrero-Hernández E., Andrades M.S., Álvarez-Martín A., Pose-Juan E., Rodríguez-Cruz M.S., Sánchez-Martín M.J., Occurrence of pesticides and some of their degradation products in waters in a Spanish wine region, J. Hydrol., 486 (2013) 234–245.
  • [21] Lemos L.S., Angarica L.M., Hauser-Davis R.A., Quinete N., Cortisol as a stress indicator in fish: Sampling methods, analytical techniques, and organic pollutant exposure assessments, International Journal of Environmental Research and Public Health, 20(13) (2023).
  • [22] Kumar N., Ambasankar K., Krishnani K., Gupta S., Bhushan S., Minhas P., Acute toxicity, biochemical, and histopathological responses of endosulfan in Chanos chanos, Ecotoxicology and Environmental Safety, 131 (2016) 79–88.
  • [23] Suvetha L., Saravanan M., Hur J.H., Ramesh M., Krishnapriya K., Acute and sublethal intoxication of deltamethrin in an Indian major carp, Labeo rohita: Hormonal and enzymological responses, Journal of Basic and Applied Zoology, 72 (2015) 58–65.
  • [24] Ghayyur S., Tabassum S., Ahmad M.S., Akhtar N., Khan M.F., Effect of chlorpyrifos on hematological and seral biochemical components of fish Oreochromis niloticus, Pakistan Journal of Zoology, 51(3) (2019) 1047–1052.
  • [25] Chadwick J.G., Nislow K.H., McCormick S.D., Thermal onset of cellular and endocrine stress responses correspond to ecological limits in brook trout, Conservation Physiology, 3(1) (2015) cov017.
  • [26] Gandar A., Laffaille P., Canlet C., Trembay-Franco M., Gautier R., Perrault A., Gress L., Mormede P., Tapie N., Budzinski H., Jean S., Adaptive response under multiple stress exposures in fish: From the molecular to the individual level, Chemosphere, 188 (2017) 60–72.
  • [27] Alix M., Kjesbu O.S., Anderson K.C., From gametogenesis to spawning: How climate-driven warming affects teleost reproductive biology, Fish Biology, 97(3) (2020) 607–632.
  • [28] Servili A., Canario A.V.M., Mouchel O., Munoz-Cueto J.A., Climate change impacts on fish reproduction are mediated at multiple levels of the brain-pituitary-gonad axis, General and Comparative Endocrinology, 291 (2020) 113439.
  • [29] Pankhurst N.W., Thomas P.M., Maintenance at elevated temperature delays the steroidogenic and ovulatory responsiveness of rainbow trout (Oncorhynchus mykiss) to luteinizing hormone-releasing hormone analogue, Aquaculture, 166(1–2) (1998) 163–177.
  • [30] Guo D., Liu W., Qiu J., Li Y., Chen L., Wu S., Qian Y., Changes in thyroid hormone levels and related gene expressions in embryo-larval zebrafish exposed to binary combinations of bifenthrin and acetochlor, Ecotoxicology, 29(5) (2020) 584–593.
  • [31] Kongtip P., Nankongnab N., Pundee R., Kallayanatham N., Pengpumkiat S., Chungcharoen J., Woskie S., Acute changes in thyroid hormone levels among Thai pesticide sprayers, Toxics, 9(1) (2021).
  • [32] Little A.G., Kunisue T., Kannan K., Seebacher F., Thyroid hormone actions are temperature-specific and regulate thermal acclimation in zebrafish (Danio rerio), BMC Biology, 11 (2013) 26.
  • [33] Samanta P., Pal S., Mukherjee A.K., Ghosh A.R., Evaluation of metabolic enzymes in response to Excel Mera 71, a glyphosate-based herbicide, and recovery pattern in freshwater teleostean fishes, Biomed Research International, (2014) 425159.
  • [34] Qin H., Long Z., Huang Z., Ma J., Kong L., Lin Y., Li Z., A comparison of the physiological responses to heat stress of two sizes of juvenile spotted seabass (Lateolabrax maculatus), Fishes, 8(7) (2023) 340.
  • [35] Sapana Devi M., Gupta A., Sublethal toxicity of commercial formulations of deltamethrin and permethrin on selected biochemical constituents and enzyme activities in liver and muscle tissues of Anabas testudineus, Pesticide Biochemistry and Physiology, 115 (2014) 48–52.
  • [36] Phinrub W., Lunjirapan T., Srirum T., Kumjumrern K., Srisuttha P., Panase A., Panase P., Alterations of serum electrolytes and biochemical indices of Pangasianodon gigas subjected to different water temperatures and the appropriate temperature range for sustaining life, Journal of Applied Animal Research, 51(1) (2023) 342–349.
  • [37] Davis K.B., Temperature affects physiological stress responses to acute confinement in sunshine bass (Morone chrysops × Morone saxatilis), Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology, 139(4) (2004).
  • [38] Pillans R.D., Anderson W.G., Good J.P., Hyodo S., Takei Y., Hazon N., Franklin C.E., Plasma and erythrocyte solute properties of juvenile bull sharks (Carcharhinus leucas) acutely exposed to increasing environmental salinity, Journal of Experimental Marine Biology and Ecology, 331(2) (2006) 145–157.

Pendimetalin ve Fluometuron`a Farklı Sıcaklıklarda Maruz Kalmanın Tilapia nilotica Üzerindeki Biyokimyasal Etkileri

Year 2025, Volume: 46 Issue: 2, 250 - 256, 30.06.2025

Derya Kocamaz , Mine Beyazaslan , Aşkın Barış Kaya

https://doi.org/10.17776/csj.1630407

Abstract

İklim değişikliğine bağlı olarak sıcaklık artışı sucul sistemlerdeki pestisit toksisitesini önemli ölçüde etkilemektedir. Bu nedenle, Tilapia nilotica´da pendimethalin ve fluometuron ile sıcaklık artışına birlikte maruz kalmanın biyokimyasal etkilerini araştırdık. Balıklar, pendimethalin ve fluometuron karışımının düşük (0,1 ppb) ve yüksek (1 ppb) derişimlerine 96 saat süresince iki farklı sıcaklıkta (220C ve 280C) maruz bırakıldılar. Analiz edilen tüm parametreler için derişim ve sıcaklık arasında anlamlı etkileşim bulunmuştur. Kortizol miktarı 22 0C’de her iki derişimde kontrolle karşılaştırıldığında artarken, 28 0C’de azalmıştır. Estradiol ve testosteron düzeylerinin 28 0C’de her iki derişimde azaldığı belirlenmiştir. Ayrıca, her iki sıcaklıkta triiyodotironin ve tiroksin düzeylerinin yüksek derişimli pestisit karışımı etkisinde azaldığı belirlenmiştir. Alanin-aminotransferaz ve aspartat-aminotrasferaz düzeylerinin ise 28 0C’deki düşük derişimli pestisit karışımı hariç diğer uygulamalarda azaldığı bulunmuştur. İyon düzeylerinin ise 28 0C’de yüksek derişimli pestisit karışımı etkisinde azaldığı belirlenmiştir. Bulgularımız, yüksek sıcaklığın pendimethalin ve fluometuron'un karışım uygulamasının toksik etkisini arttırdığını göstermiştir. Bu nedenle hedef olmayan organizmaların küresel ısınmadan nasıl etkilendiğini anlayabilmek için çoklu stres faktörlerine akut maruziyetin etkilerinin ayrıntılı olarak incelenmesi önem taşımaktadır.

Keywords

Fluometuron Pendimethalin Tilapia nilotica Pestisit karışımı Küresel Isınma

References

  • [1] Muralikrishna I.V., Manickam V., Environmental Policies and Legislation, Environmental Management, (2017) 37–55.
  • [2] Noyes P.D., Lema S.C., Forecasting the impacts of chemical pollution and climate change interactions on the health of wildlife, Current Zoology, 61(4) (2015) 669–689.
  • [3] Marchand A., Haddad S., Simultaneous exposures to heat and chemicals and the impact on toxicokinetic and biomonitoring, Current Opinion in Toxicology, 4 (2017) 22–27.
  • [4] Jacquin L., Gandar A., Aguirre-Smith M., Perrault A., Le Hénaff M., De Jong L., Paris-Palacios S., Laffaille P., Jean S., High temperature aggravates the effects of pesticides in goldfish, Ecotoxicology and Environmental Safety, 172 (2019) 255–263.
  • [5] Choudhury P.P., Saha S., Dynamics of pesticides under changing climatic scenario, Environmental Monitoring and Assessment, 192(S1) (2021).
  • [6] Philippe C., Thore E.S.J., Verbesselt S., Gregoir A.F., Brendonck L., Pinceel T., Combined effects of global warming and chlorpyrifos exposure on the annual fish Nothobranchius furzeri, Ecotoxicology and Environmental Safety, 248 (2022) 114290.
  • [7] Luks A.-K., Zegarski T., Nowak K.M., Miltner A., Kästner M., Matthies M., Schmidt B., Schäffer A., Fate of Pendimethalin in Soil and Characterization of Non-Extractable Residues (Ner), Science of the Total Environment, 753 (2021).
  • [8] Vighi M., Matthies M., Solomon K.R., Critical assessment of pendimethalin in terms of persistence, bioaccumulation, toxicity, and potential for long-range transport, J. Toxicol. Environ. Health Part B, 20(1) (2016) 1–21.
  • [9] European Food Safety Authority, Peer review of the pesticide risk assessment of the active substance pendimethalin, EFSA J., (2016).
  • [10] Herrero-Hernandez E., Simon-Egea A.B., Sanchez-Martin M.J., Rodriguez-Cruz M.S., Andrades M.S., Monitoring and environmental risk assessment of pesticide residues and some of their degradation products in natural waters of the Spanish vineyard region included in the Denomination of Origin Jumilla, Environmental Pollution, 264 (2020) 114666.
  • [11] Asman W.A., Jorgensen A., Bossi R., Vejrup K.V., Mogensen B.B., Glasius M., Wet deposition of pesticides and nitrophenols at two sites in Denmark: measurements and contributions from regional sources, Chemosphere, 59(7) (2005) 1023–1031.
  • [12] Barba-Brioso C., Fernandez-Caliani J.C., Miras A., Cornejo J., Galan E., Multi-source water pollution in a highly anthropized wetland system associated with the estuary of Huelva (SW Spain), Marine Pollution Bulletin, 60(8) (2010) 1259–1269.
  • [13] Udarbe Zamora E., Fluometuron, Encyclopedia of Toxicology, 340–342 (2005).
  • [14] Gikas G.D., Vryzas Z., Koshis Z., Experiments on fluometuron removal from simulated agricultural wastewater in porous media filters, Environ. Process., 9(1) (2021).
  • [15] Coupe R.H., Welch H.L., Pell A.B., Thurman E.M., Herbicide and degradate flux in the Yazoo River Basin, Int. J. Environ. Anal. Chem., 85 (2005) 1127–1140 [16] U.S. E.P.A., Chemical Information Fact Sheet Number 88: Fluometuron, Office of Pesticides and Toxic Substances, Washington, DC (1985).
  • [16] de Almeida M.D., Pereira T.S.B., Batlouni S.R., Boscolo C.N.P., de Almeida E.A., Estrogenic and anti-androgenic effects of the herbicide tebuthiuron in male Nile tilapia (Oreochromis niloticus), Aquatic Toxicology, 194 (2018) 86–93
  • [17] Maharaj S., El Ahmadie N., Rheingold S., El Chehouri J., Yang L., Souders C.L., Martyniuk C.J., Sub-lethal toxicity assessment of the phenylurea herbicide linuron in developing zebrafish (Danio rerio) embryo/larvae, Neurotoxicology Teratology, 81 (2020) 106917.
  • [18] Bojarski B.L., Swadźba-Karbowy M., Makulska J., Jakubiak M., Pawlak K., Tombarkiewicz B., Witeska M., Effects of herbicides pendimethalin and ethofumesate on common carp (Cyprinus carpio) erythrocyte morphology, Folia Biologica, 66(3) (2018) 143–149.
  • [19] Gupta P., Verma S.K., Impacts of herbicide pendimethalin on sex steroid level, plasma vitellogenin concentration and aromatase activity in teleost Clarias batrachus (Linnaeus), Environmental Toxicology and Pharmacology, 75 (2020) 103324.
  • [20] Herrero-Hernández E., Andrades M.S., Álvarez-Martín A., Pose-Juan E., Rodríguez-Cruz M.S., Sánchez-Martín M.J., Occurrence of pesticides and some of their degradation products in waters in a Spanish wine region, J. Hydrol., 486 (2013) 234–245.
  • [21] Lemos L.S., Angarica L.M., Hauser-Davis R.A., Quinete N., Cortisol as a stress indicator in fish: Sampling methods, analytical techniques, and organic pollutant exposure assessments, International Journal of Environmental Research and Public Health, 20(13) (2023).
  • [22] Kumar N., Ambasankar K., Krishnani K., Gupta S., Bhushan S., Minhas P., Acute toxicity, biochemical, and histopathological responses of endosulfan in Chanos chanos, Ecotoxicology and Environmental Safety, 131 (2016) 79–88.
  • [23] Suvetha L., Saravanan M., Hur J.H., Ramesh M., Krishnapriya K., Acute and sublethal intoxication of deltamethrin in an Indian major carp, Labeo rohita: Hormonal and enzymological responses, Journal of Basic and Applied Zoology, 72 (2015) 58–65.
  • [24] Ghayyur S., Tabassum S., Ahmad M.S., Akhtar N., Khan M.F., Effect of chlorpyrifos on hematological and seral biochemical components of fish Oreochromis niloticus, Pakistan Journal of Zoology, 51(3) (2019) 1047–1052.
  • [25] Chadwick J.G., Nislow K.H., McCormick S.D., Thermal onset of cellular and endocrine stress responses correspond to ecological limits in brook trout, Conservation Physiology, 3(1) (2015) cov017.
  • [26] Gandar A., Laffaille P., Canlet C., Trembay-Franco M., Gautier R., Perrault A., Gress L., Mormede P., Tapie N., Budzinski H., Jean S., Adaptive response under multiple stress exposures in fish: From the molecular to the individual level, Chemosphere, 188 (2017) 60–72.
  • [27] Alix M., Kjesbu O.S., Anderson K.C., From gametogenesis to spawning: How climate-driven warming affects teleost reproductive biology, Fish Biology, 97(3) (2020) 607–632.
  • [28] Servili A., Canario A.V.M., Mouchel O., Munoz-Cueto J.A., Climate change impacts on fish reproduction are mediated at multiple levels of the brain-pituitary-gonad axis, General and Comparative Endocrinology, 291 (2020) 113439.
  • [29] Pankhurst N.W., Thomas P.M., Maintenance at elevated temperature delays the steroidogenic and ovulatory responsiveness of rainbow trout (Oncorhynchus mykiss) to luteinizing hormone-releasing hormone analogue, Aquaculture, 166(1–2) (1998) 163–177.
  • [30] Guo D., Liu W., Qiu J., Li Y., Chen L., Wu S., Qian Y., Changes in thyroid hormone levels and related gene expressions in embryo-larval zebrafish exposed to binary combinations of bifenthrin and acetochlor, Ecotoxicology, 29(5) (2020) 584–593.
  • [31] Kongtip P., Nankongnab N., Pundee R., Kallayanatham N., Pengpumkiat S., Chungcharoen J., Woskie S., Acute changes in thyroid hormone levels among Thai pesticide sprayers, Toxics, 9(1) (2021).
  • [32] Little A.G., Kunisue T., Kannan K., Seebacher F., Thyroid hormone actions are temperature-specific and regulate thermal acclimation in zebrafish (Danio rerio), BMC Biology, 11 (2013) 26.
  • [33] Samanta P., Pal S., Mukherjee A.K., Ghosh A.R., Evaluation of metabolic enzymes in response to Excel Mera 71, a glyphosate-based herbicide, and recovery pattern in freshwater teleostean fishes, Biomed Research International, (2014) 425159.
  • [34] Qin H., Long Z., Huang Z., Ma J., Kong L., Lin Y., Li Z., A comparison of the physiological responses to heat stress of two sizes of juvenile spotted seabass (Lateolabrax maculatus), Fishes, 8(7) (2023) 340.
  • [35] Sapana Devi M., Gupta A., Sublethal toxicity of commercial formulations of deltamethrin and permethrin on selected biochemical constituents and enzyme activities in liver and muscle tissues of Anabas testudineus, Pesticide Biochemistry and Physiology, 115 (2014) 48–52.
  • [36] Phinrub W., Lunjirapan T., Srirum T., Kumjumrern K., Srisuttha P., Panase A., Panase P., Alterations of serum electrolytes and biochemical indices of Pangasianodon gigas subjected to different water temperatures and the appropriate temperature range for sustaining life, Journal of Applied Animal Research, 51(1) (2023) 342–349.
  • [37] Davis K.B., Temperature affects physiological stress responses to acute confinement in sunshine bass (Morone chrysops × Morone saxatilis), Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology, 139(4) (2004).
  • [38] Pillans R.D., Anderson W.G., Good J.P., Hyodo S., Takei Y., Hazon N., Franklin C.E., Plasma and erythrocyte solute properties of juvenile bull sharks (Carcharhinus leucas) acutely exposed to increasing environmental salinity, Journal of Experimental Marine Biology and Ecology, 331(2) (2006) 145–157.
There are 38 citations in total.

Details

Primary Language English
Subjects Ecotoxicology
Journal Section Natural Sciences
Authors

Derya Kocamaz 0000-0002-0705-4672

Mine Beyazaslan 0009-0008-3899-0288

Aşkın Barış Kaya 0009-0001-9274-7237

Publication Date June 30, 2025
Submission Date January 31, 2025
Acceptance Date May 11, 2025
Published in Issue Year 2025Volume: 46 Issue: 2

Cite

APA Kocamaz, D., Beyazaslan, M., & Kaya, A. B. (2025). Temperature-Dependent Biochemical Alterations in Oreochromis niloticus exposed to Pendimethalin and Fluometuron. Cumhuriyet Science Journal, 46(2), 250-256. https://doi.org/10.17776/csj.1630407