TY - JOUR
T1 - Developmental assays using invasive cane toads, Rhinella marina, reveal safety concerns of a common formulation of the rice herbicide, butachlor
AU - Shuman-Goodier, Molly E.
AU - Singleton, Grant R.
AU - Forsman, Anna M.
AU - Hines, Shyann
AU - Christodoulides, Nicholas
AU - Daniels, Kevin D.
AU - Propper, Catherine R.
N1 - Funding Information:
We thank Alexander McCain, Morgan Jones, and Calsey Richardson and Phoebe Shuman-Goodier for their assistance in the field and laboratory. We also thank Loren Buck, Stephen Shuster, and Rachel Rubin for their editorial support, Mark Loftus and Sayf Hassouneh for their assistance with using Hisat2, and the anonymous reviewers who helped to improve the manuscript. Funding was provided by the Merriam Powell Center for Environmental Research’s Integrative Graduate Education, Research, and Traineeship Program (IGERT) Fellowship, an Early Career Grant to MSG from the National Geographic Society, the Achievement Rewards for College Scientists (ARCS) Foundation, the Closing Rice Yield Gaps in Asia with a Reduced Environmental Footprint (CORIGAP) funded by the Swiss Agency for Development and Cooperation through the International Rice Research Institute (Grant Number 81046615), and the National Institute on Minority Health and Health Disparities of the NIH (Award Number T37MD008626 to CRP).
Funding Information:
We thank Alexander McCain, Morgan Jones, and Calsey Richardson and Phoebe Shuman-Goodier for their assistance in the field and laboratory. We also thank Loren Buck, Stephen Shuster, and Rachel Rubin for their editorial support, Mark Loftus and Sayf Hassouneh for their assistance with using Hisat2, and the anonymous reviewers who helped to improve the manuscript. Funding was provided by the Merriam Powell Center for Environmental Research's Integrative Graduate Education, Research, and Traineeship Program (IGERT) Fellowship, an Early Career Grant to MSG from the National Geographic Society, the Achievement Rewards for College Scientists (ARCS) Foundation, the Closing Rice Yield Gaps in Asia with a Reduced Environmental Footprint (CORIGAP) funded by the Swiss Agency for Development and Cooperation through the International Rice Research Institute (Grant Number 81046615), and the National Institute on Minority Health and Health Disparities of the NIH (Award Number T37MD008626 to CRP).
Publisher Copyright:
© 2020
PY - 2021/3/1
Y1 - 2021/3/1
N2 - 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. 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.
AB - 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. 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.
KW - Amphibians
KW - Butachlor
KW - Cane toad
KW - Endocrine disruption
KW - Machete
KW - Pesticide
KW - Rice
KW - Thyroid
KW - Transcriptome
UR - http://www.scopus.com/inward/record.url?scp=85096452572&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85096452572&partnerID=8YFLogxK
U2 - 10.1016/j.envpol.2020.115955
DO - 10.1016/j.envpol.2020.115955
M3 - Article
C2 - 33221087
AN - SCOPUS:85096452572
SN - 0269-7491
VL - 272
JO - Environmental Pollution
JF - Environmental Pollution
M1 - 115955
ER -