Developmental assays using invasive cane toads, Rhinella marina, reveal safety concerns of a common formulation of the rice herbicide, butachlor
Identifying the adverse impacts of pesticide exposure is essential to guide regulations that are protective of wildlife and human health. Within rice ecosystems, amphibians are valuable indicators because pesticide applications coincide with sensitive reproductive and developmental life stages. We c...
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Published in: | Environmental pollution (1987) Vol. 272; p. 115955 |
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Abstract | Identifying the adverse impacts of pesticide exposure is essential to guide regulations that are protective of wildlife and human health. Within rice ecosystems, amphibians are valuable indicators because pesticide applications coincide with sensitive reproductive and developmental life stages. We conducted two experiments using wild cane toads (Rhinella marina) to test 1) whether environmentally relevant exposure to a commercial formulation of butachlor, an acetanilide herbicide used extensively in rice, affects amphibian development and 2) whether cane toad tadpoles are capable of acclimatizing to sub-lethal exposure. First, we exposed wild cane toads to 0.002, 0.02, or 0.2 mg/L of butachlor (Machete EC), during distinct development stages (as eggs and hatchlings, as tadpoles, or continuously) for 12 days. Next, we exposed a subset of animals from the first experiment to a second, lethal concentration and examined survivorship. We found that cane toads exposed to butachlor developed slower and weighed less than controls, and that development of the thyroid gland was affected: exposed individuals had smaller thyroid glands and thyrocyte cells, and more individual follicles. Analyses of the transcriptome revealed that butachlor exposure resulted in downregulation of transcripts related to metabolic processes, anatomic structure development, immune system function, and response to stress. Last, we observed evidence of acclimatization, where animals exposed to butachlor early in life performed better than naïve animals during a second exposure. Our findings indicate that the commercial formulation of butachlor, Machete EC, causes thyroid endocrine disruption in vertebrates, and suggest that exposure in lowland irrigated rice fields presents a concern for wildlife and human health. Furthermore, we establish that developmental assays with cane toads can be used to screen for adverse effects of pesticides in rice fields.
[Display omitted]
•Realistic exposure to butachlor affected development of cane toad tadpoles.•Animals developed slower, weighed less, and the thyroid gland was affected.•Non-monotonic response; low concentration, 0.002 mg/L, produced the largest effects.•Exposure caused extensive downregulation of transcripts.•Cane toad tadpoles can acclimatize to some herbicide exposures.
Environmentally relevant exposures to a commercial formulation of butachlor, an herbicide used extensively in rice, affect development, morphology, and gene expression of cane toad tadpoles. Developmental assays with cane toad tadpoles can be used to screen for adverse effects of pesticides in rice fields. |
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AbstractList | Identifying the adverse impacts of pesticide exposure is essential to guide regulations that are protective of wildlife and human health. Within rice ecosystems, amphibians are valuable indicators because pesticide applications coincide with sensitive reproductive and developmental life stages. We conducted two experiments using wild cane toads (Rhinella marina) to test 1) whether environmentally relevant exposure to a commercial formulation of butachlor, an acetanilide herbicide used extensively in rice, affects amphibian development and 2) whether cane toad tadpoles are capable of acclimatizing to sub-lethal exposure. First, we exposed wild cane toads to 0.002, 0.02, or 0.2 mg/L of butachlor (Machete EC), during distinct development stages (as eggs and hatchlings, as tadpoles, or continuously) for 12 days. Next, we exposed a subset of animals from the first experiment to a second, lethal concentration and examined survivorship. We found that cane toads exposed to butachlor developed slower and weighed less than controls, and that development of the thyroid gland was affected: exposed individuals had smaller thyroid glands and thyrocyte cells, and more individual follicles. Analyses of the transcriptome revealed that butachlor exposure resulted in downregulation of transcripts related to metabolic processes, anatomic structure development, immune system function, and response to stress. Last, we observed evidence of acclimatization, where animals exposed to butachlor early in life performed better than naïve animals during a second exposure. Our findings indicate that the commercial formulation of butachlor, Machete EC, causes thyroid endocrine disruption in vertebrates, and suggest that exposure in lowland irrigated rice fields presents a concern for wildlife and human health. Furthermore, we establish that developmental assays with cane toads can be used to screen for adverse effects of pesticides in rice fields. Identifying the adverse impacts of pesticide exposure is essential to guide regulations that are protective of wildlife and human health. Within rice ecosystems, amphibians are valuable indicators because pesticide applications coincide with sensitive reproductive and developmental life stages. We conducted two experiments using wild cane toads (Rhinella marina) to test 1) whether environmentally relevant exposure to a commercial formulation of butachlor, an acetanilide herbicide used extensively in rice, affects amphibian development and 2) whether cane toad tadpoles are capable of acclimatizing to sub-lethal exposure. First, we exposed wild cane toads to 0.002, 0.02, or 0.2 mg/L of butachlor (Machete EC), during distinct development stages (as eggs and hatchlings, as tadpoles, or continuously) for 12 days. Next, we exposed a subset of animals from the first experiment to a second, lethal concentration and examined survivorship. We found that cane toads exposed to butachlor developed slower and weighed less than controls, and that development of the thyroid gland was affected: exposed individuals had smaller thyroid glands and thyrocyte cells, and more individual follicles. Analyses of the transcriptome revealed that butachlor exposure resulted in downregulation of transcripts related to metabolic processes, anatomic structure development, immune system function, and response to stress. Last, we observed evidence of acclimatization, where animals exposed to butachlor early in life performed better than naïve animals during a second exposure. Our findings indicate that the commercial formulation of butachlor, Machete EC, causes thyroid endocrine disruption in vertebrates, and suggest that exposure in lowland irrigated rice fields presents a concern for wildlife and human health. Furthermore, we establish that developmental assays with cane toads can be used to screen for adverse effects of pesticides in rice fields. [Display omitted] •Realistic exposure to butachlor affected development of cane toad tadpoles.•Animals developed slower, weighed less, and the thyroid gland was affected.•Non-monotonic response; low concentration, 0.002 mg/L, produced the largest effects.•Exposure caused extensive downregulation of transcripts.•Cane toad tadpoles can acclimatize to some herbicide exposures. Environmentally relevant exposures to a commercial formulation of butachlor, an herbicide used extensively in rice, affect development, morphology, and gene expression of cane toad tadpoles. Developmental assays with cane toad tadpoles can be used to screen for adverse effects of pesticides in rice fields. Identifying the adverse impacts of pesticide exposure in rice ecosystems is essential to guide regulations that are protective of wildlife and human health. Amphibians are valuable indicators within rice ecosystems because pesticide applications coincide with sensitive reproductive and developmental life stages. We conducted two experiments using wild cane toads ( Rhinella marina ) to test 1) whether environmentally relevant exposure to a commercial formulation of butachlor, an acetanilide herbicide used extensively in rice, affects amphibian development and 2) whether cane toad tadpoles are capable of acclimatizing to sub-lethal exposure. First, we exposed wild cane toads to 0.002, 0.02, or 0.2 mg/L of butachlor (Machete EC), during distinct development stages (as eggs and hatchlings, as tadpoles, or continuously) for 12 days. Next, we exposed a subset of animals from the first experiment to a second, lethal concentration and examined survivorship. We found that cane toads exposed to butachlor developed slower and weighed less than controls, and that development of the thyroid gland was affected: exposed individuals had smaller thyroid glands and thyrocyte cells, and more individual follicles. Analyses of the transcriptome revealed that butachlor exposure resulted in downregulation of transcripts related to metabolic processes, anatomic structure development, immune system function, and response to stress. Last, we observed evidence of acclimatization, where animals exposed to butachlor early in life performed better than naive animals during a second exposure. Our findings indicate that the commercial formulation of butachlor, Machete EC, causes thyroid endocrine disruption in vertebrates, and suggest that exposure in lowland irrigated rice fields presents a concern for wildlife and human health. Furthermore, we establish that developmental assays with cane toads can be used to screen for adverse effects of pesticides in rice fields. Environmentally relevant exposures to a commercial formulation of butachlor, an herbicide used extensively in rice, affect development, morphology, and gene expression of cane toad tadpoles. Developmental assays with cane toad tadpoles can be used to screen for adverse effects of pesticides in rice fields. |
ArticleNumber | 115955 |
Author | Forsman, Anna M. Singleton, Grant R. Daniels, Kevin D. Shuman-Goodier, Molly E. Propper, Catherine R. Hines, Shyann Christodoulides, Nicholas |
AuthorAffiliation | a Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86001 b International Rice Research Institute, Los Baños, Philippines e Genomics and Bioinformatics Cluster, University of Central Florida, Orlando, FL 32816-2368 c Natural Resource Institute, University of Greenwich, Chatham Maritime, Kent, UK f Department of Chemical and Environmental Engineering, University of Arizona, Tucson, AZ 85721 d Department of Biology, University of Central Florida, Orlando, FL 32816-2368 |
AuthorAffiliation_xml | – name: f Department of Chemical and Environmental Engineering, University of Arizona, Tucson, AZ 85721 – name: b International Rice Research Institute, Los Baños, Philippines – name: e Genomics and Bioinformatics Cluster, University of Central Florida, Orlando, FL 32816-2368 – name: a Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ 86001 – name: c Natural Resource Institute, University of Greenwich, Chatham Maritime, Kent, UK – name: d Department of Biology, University of Central Florida, Orlando, FL 32816-2368 |
Author_xml | – sequence: 1 givenname: Molly E. surname: Shuman-Goodier fullname: Shuman-Goodier, Molly E. email: ms2883@nau.edu organization: Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, 86001, USA – sequence: 2 givenname: Grant R. orcidid: 0000-0002-2154-1223 surname: Singleton fullname: Singleton, Grant R. organization: International Rice Research Institute, Los Baños, Philippines – sequence: 3 givenname: Anna M. surname: Forsman fullname: Forsman, Anna M. organization: Department of Biology, University of Central Florida, Orlando, FL, 32816-2368, USA – sequence: 4 givenname: Shyann surname: Hines fullname: Hines, Shyann organization: Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, 86001, USA – sequence: 5 givenname: Nicholas orcidid: 0000-0001-7371-6550 surname: Christodoulides fullname: Christodoulides, Nicholas organization: Department of Biology, University of Central Florida, Orlando, FL, 32816-2368, USA – sequence: 6 givenname: Kevin D. orcidid: 0000-0002-2857-7421 surname: Daniels fullname: Daniels, Kevin D. organization: Department of Chemical and Environmental Engineering, University of Arizona, Tucson, AZ, 85721, USA – sequence: 7 givenname: Catherine R. surname: Propper fullname: Propper, Catherine R. organization: Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, 86001, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33221087$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1080_15287394_2023_2224366 crossref_primary_10_1016_j_hazadv_2023_100275 crossref_primary_10_1016_j_etap_2022_103910 crossref_primary_10_1080_10937404_2022_2140372 crossref_primary_10_1016_j_envres_2022_115104 crossref_primary_10_1002_csc2_20564 crossref_primary_10_1111_gcb_17137 crossref_primary_10_1007_s00253_021_11346_3 crossref_primary_10_1016_j_crope_2023_11_005 crossref_primary_10_3389_fceng_2022_721923 crossref_primary_10_1016_j_foodchem_2024_139215 |
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Keywords | Butachlor Cane toad Machete Pesticide Transcriptome Endocrine disruption Amphibians Rice Thyroid |
Language | English |
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Notes | Molly E. Shuman Goodier: Conceptualization, Methodology, Data collection and curation, Visualization, Analyses, Writing (original and final preparation), Funding acquisition Grant R. Singleton: Supervision, Conceptualization, Writing – editing, Funding acquisition Catherine R. Propper: Supervision, Conceptualization, Writing, Funding acquisition Nicholas Christodoulides: Methodology & Data curation (DE and GO analyses) Anna M. Forsman: Methodology, Data curation & Writing (RNAseq) Shyann Hines: Methodology (thyroid data curation) Kevin D. Daniels: Methodology, Writing (butachlor quantification) |
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SubjectTerms | Acetanilides - toxicity Amphibians Animals Bufo marinus Butachlor Cane toad Ecosystem Endocrine disruption Herbicides - toxicity Humans Introduced Species Machete Oryza Pesticide Rice Thyroid Transcriptome |
Title | Developmental assays using invasive cane toads, Rhinella marina, reveal safety concerns of a common formulation of the rice herbicide, butachlor |
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