Developmental exposure to environmentally relevant concentrations of bifenthrin alters transcription of mTOR and ryanodine receptor-dependent signaling molecules and impairs predator avoidance behavior across early life stages in inland silversides (Menidia beryllina)

Daniel F. Frank, Susanne M. Brander, Simone Hasenbein, Danielle J Harvey, Pamela J Lein, Juergen Geist, Richard E Connon

Research output: Contribution to journalArticle

Abstract

Altered transcription of calcium-dependent signaling cascades involving the ryanodine receptor (RyR) and mechanistic target of rapamycin (mTOR) in response to environmental exposures have been described in model vertebrates, including zebrafish, while the relevance for wild fishes remains unknown. To address this knowledge gap, we exposed the euryhaline model species Menidia beryllina (inland silversides) to the insecticide bifenthrin, a known modulator of calcium signaling. The main objectives of this study were to determine: (1) whether exposure of developing silversides to environmentally relevant concentrations of bifenthrin alters their behavior; and (2) whether behavioral changes correlate with altered expression of genes involved in RyR and mTOR-dependent signaling pathways. At six hours post fertilization (hpf), inland silversides were exposed to bifenthrin at 3, 27 and 122 ng/L until 7 days post fertilization (dpf, larvae hatched at 6dpf), followed by a 14-day recovery period in uncontaminated water. Transcriptional responses were measured at 5, 7 and 21 dpf; locomotor behavior following external stimuli and response to an olfactory predator cue were assessed at 7 and 21 dpf. Bifenthrin elicited significant non-monotonic transcriptional responses in the majority of genes examined at 5 dpf and at 21 dpf. Bifenthrin also significantly altered predator avoidance behavior via olfactory mechanisms with main effects identified for animals exposed to 3 and 27 ng/L. Behavioral effects were not detected in response to visual stimuli during acute exposure, but were significant in the predator-cue assessment following the recovery period, suggesting delayed and long-term effects of early developmental exposures to bifenthrin. Our findings demonstrate that at picomolar (pM) concentrations, which are often not represented in ecotoxicological studies, bifenthrin perturbs early development of inland silversides. These developmental impacts are manifested behaviorally at later life stages, specifically as altered patterns of predator avoidance behavior, which have been correlated with population decline. Collectively, these data suggest that bifenthrin may be negatively impacting wild fish populations.

LanguageEnglish (US)
Pages1-13
Number of pages13
JournalAquatic Toxicology
Volume206
DOIs
StatePublished - Jan 1 2019

Fingerprint

bifenthrin
Avoidance Learning
ryanodine receptors
Ryanodine Receptor Calcium Release Channel
avoidance behavior
Sirolimus
transcription (genetics)
predator
predators
Calcium Signaling
wild fish
Fertilization
Cues
Fishes
calcium
acute exposure
visual cue
Menidia beryllina
exposure
gene

Keywords

  • Ca2+-dependent signaling
  • Fish behavior
  • Insecticide
  • Neurodevelopment
  • Pesticide
  • Pyrethroid

ASJC Scopus subject areas

  • Aquatic Science
  • Health, Toxicology and Mutagenesis

Cite this

@article{2615916c44c24b64bf147ed37fdc8646,
title = "Developmental exposure to environmentally relevant concentrations of bifenthrin alters transcription of mTOR and ryanodine receptor-dependent signaling molecules and impairs predator avoidance behavior across early life stages in inland silversides (Menidia beryllina)",
abstract = "Altered transcription of calcium-dependent signaling cascades involving the ryanodine receptor (RyR) and mechanistic target of rapamycin (mTOR) in response to environmental exposures have been described in model vertebrates, including zebrafish, while the relevance for wild fishes remains unknown. To address this knowledge gap, we exposed the euryhaline model species Menidia beryllina (inland silversides) to the insecticide bifenthrin, a known modulator of calcium signaling. The main objectives of this study were to determine: (1) whether exposure of developing silversides to environmentally relevant concentrations of bifenthrin alters their behavior; and (2) whether behavioral changes correlate with altered expression of genes involved in RyR and mTOR-dependent signaling pathways. At six hours post fertilization (hpf), inland silversides were exposed to bifenthrin at 3, 27 and 122 ng/L until 7 days post fertilization (dpf, larvae hatched at 6dpf), followed by a 14-day recovery period in uncontaminated water. Transcriptional responses were measured at 5, 7 and 21 dpf; locomotor behavior following external stimuli and response to an olfactory predator cue were assessed at 7 and 21 dpf. Bifenthrin elicited significant non-monotonic transcriptional responses in the majority of genes examined at 5 dpf and at 21 dpf. Bifenthrin also significantly altered predator avoidance behavior via olfactory mechanisms with main effects identified for animals exposed to 3 and 27 ng/L. Behavioral effects were not detected in response to visual stimuli during acute exposure, but were significant in the predator-cue assessment following the recovery period, suggesting delayed and long-term effects of early developmental exposures to bifenthrin. Our findings demonstrate that at picomolar (pM) concentrations, which are often not represented in ecotoxicological studies, bifenthrin perturbs early development of inland silversides. These developmental impacts are manifested behaviorally at later life stages, specifically as altered patterns of predator avoidance behavior, which have been correlated with population decline. Collectively, these data suggest that bifenthrin may be negatively impacting wild fish populations.",
keywords = "Ca2+-dependent signaling, Fish behavior, Insecticide, Neurodevelopment, Pesticide, Pyrethroid",
author = "Frank, {Daniel F.} and Brander, {Susanne M.} and Simone Hasenbein and Harvey, {Danielle J} and Lein, {Pamela J} and Juergen Geist and Connon, {Richard E}",
year = "2019",
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T1 - Developmental exposure to environmentally relevant concentrations of bifenthrin alters transcription of mTOR and ryanodine receptor-dependent signaling molecules and impairs predator avoidance behavior across early life stages in inland silversides (Menidia beryllina)

AU - Frank, Daniel F.

AU - Brander, Susanne M.

AU - Hasenbein, Simone

AU - Harvey, Danielle J

AU - Lein, Pamela J

AU - Geist, Juergen

AU - Connon, Richard E

PY - 2019/1/1

Y1 - 2019/1/1

N2 - Altered transcription of calcium-dependent signaling cascades involving the ryanodine receptor (RyR) and mechanistic target of rapamycin (mTOR) in response to environmental exposures have been described in model vertebrates, including zebrafish, while the relevance for wild fishes remains unknown. To address this knowledge gap, we exposed the euryhaline model species Menidia beryllina (inland silversides) to the insecticide bifenthrin, a known modulator of calcium signaling. The main objectives of this study were to determine: (1) whether exposure of developing silversides to environmentally relevant concentrations of bifenthrin alters their behavior; and (2) whether behavioral changes correlate with altered expression of genes involved in RyR and mTOR-dependent signaling pathways. At six hours post fertilization (hpf), inland silversides were exposed to bifenthrin at 3, 27 and 122 ng/L until 7 days post fertilization (dpf, larvae hatched at 6dpf), followed by a 14-day recovery period in uncontaminated water. Transcriptional responses were measured at 5, 7 and 21 dpf; locomotor behavior following external stimuli and response to an olfactory predator cue were assessed at 7 and 21 dpf. Bifenthrin elicited significant non-monotonic transcriptional responses in the majority of genes examined at 5 dpf and at 21 dpf. Bifenthrin also significantly altered predator avoidance behavior via olfactory mechanisms with main effects identified for animals exposed to 3 and 27 ng/L. Behavioral effects were not detected in response to visual stimuli during acute exposure, but were significant in the predator-cue assessment following the recovery period, suggesting delayed and long-term effects of early developmental exposures to bifenthrin. Our findings demonstrate that at picomolar (pM) concentrations, which are often not represented in ecotoxicological studies, bifenthrin perturbs early development of inland silversides. These developmental impacts are manifested behaviorally at later life stages, specifically as altered patterns of predator avoidance behavior, which have been correlated with population decline. Collectively, these data suggest that bifenthrin may be negatively impacting wild fish populations.

AB - Altered transcription of calcium-dependent signaling cascades involving the ryanodine receptor (RyR) and mechanistic target of rapamycin (mTOR) in response to environmental exposures have been described in model vertebrates, including zebrafish, while the relevance for wild fishes remains unknown. To address this knowledge gap, we exposed the euryhaline model species Menidia beryllina (inland silversides) to the insecticide bifenthrin, a known modulator of calcium signaling. The main objectives of this study were to determine: (1) whether exposure of developing silversides to environmentally relevant concentrations of bifenthrin alters their behavior; and (2) whether behavioral changes correlate with altered expression of genes involved in RyR and mTOR-dependent signaling pathways. At six hours post fertilization (hpf), inland silversides were exposed to bifenthrin at 3, 27 and 122 ng/L until 7 days post fertilization (dpf, larvae hatched at 6dpf), followed by a 14-day recovery period in uncontaminated water. Transcriptional responses were measured at 5, 7 and 21 dpf; locomotor behavior following external stimuli and response to an olfactory predator cue were assessed at 7 and 21 dpf. Bifenthrin elicited significant non-monotonic transcriptional responses in the majority of genes examined at 5 dpf and at 21 dpf. Bifenthrin also significantly altered predator avoidance behavior via olfactory mechanisms with main effects identified for animals exposed to 3 and 27 ng/L. Behavioral effects were not detected in response to visual stimuli during acute exposure, but were significant in the predator-cue assessment following the recovery period, suggesting delayed and long-term effects of early developmental exposures to bifenthrin. Our findings demonstrate that at picomolar (pM) concentrations, which are often not represented in ecotoxicological studies, bifenthrin perturbs early development of inland silversides. These developmental impacts are manifested behaviorally at later life stages, specifically as altered patterns of predator avoidance behavior, which have been correlated with population decline. Collectively, these data suggest that bifenthrin may be negatively impacting wild fish populations.

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KW - Pyrethroid

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