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Ecotoxicol Environ Saf
2023 Jul 01;259:115021. doi: 10.1016/j.ecoenv.2023.115021.
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Effects of Herbicides and the Chytrid Fungus Batrachochytrium dendrobatidis on the growth, development and survival of Larval American Toads (Anaxyrus americanus).
Paetow LJ
,
Cue RI
,
Pauli BD
,
Marcogliese DJ
.
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Pesticides and pathogens adversely affect amphibian health, but their interactive effects are not well known. We assessed independent and combined effects of two agricultural herbicides and the fungal pathogen Batrachochytrium dendrobatidis (Bd) on the growth, development and survival of larval American toads (Anaxyrus americanus). Wild-caught tadpoles were exposed to four concentrations of atrazine (0.18, 1.8, 18.0, 180 μg/L) or glyphosate (7, 70, 700, 7000 µg a.e./L), respectively contained in Aatrex® Liquid 480 (Syngenta) or Vision® Silviculture Herbicide (Monsanto) for 14 days, followed by two doses of Bd. At day 14, atrazine had not affected survival, but it non-monotonically affected growth. Exposure to the highest concentration of glyphosate caused 100% mortality within 4 days, while lower doses had an increasing monotonic effect on growth. At day 65, tadpole survival was unaffected by atrazine and the lower doses of glyphosate. Neither herbicide demonstrated an interaction effect with Bd on survival, but exposure to Bd increased survival among both herbicide-exposed and herbicide-control tadpoles. At day 60, tadpoles exposed to the highest concentration of atrazine remained smaller than controls, indicating longer-term effects of atrazine on growth, but effects of glyphosate on growth disappeared. Growth was unaffected by any herbicide-fungal interaction but was positively affected by exposure to Bd following exposure to atrazine. Atrazine exhibited a slowing and non-monotonic effect on Gosner developmental stage, while exposure to Bd tended to speed up development and act antagonistically toward the observed effect of atrazine. Overall, atrazine, glyphosate and Bd all showed a potential to modulate larval toad growth and development.
Fig. 1. Longer-term Kaplan-Meier survival curves of larval American toads (Anaxyrus americanus) showing significant independent effects (when P < 0.05) of exposure to different concentrations of either (a) atrazine (Aatrex® Liquid 480), or (b) glyphosate (Vision® Silviculture Herbicide), for the first 14 days of the experiment, and also of subsequent exposure to the chytrid fungus Batrachochytrium dendrobatidis (Bd), when tadpoles were first exposed to either (c) atrazine or (d) glyphosate. Mean survival time ( ± SE) of tadpoles exposed to 7000 µg a.e./L of glyphosate was 1.8 ± 0.3 days. * (P < 0.0001 vs controls). Exposure to Bd significantly increased survival among tadpoles pre-exposed to either atrazine ** or glyphosate ## (P < 0.0001 vs Bd controls).
Fig. 2. Effects (LSMEANS) of a 14-day exposure to different concentrations of either (a) atrazine (Aatrex® Liquid 480) or (b) glyphosate (Vision® Silviculture Herbicide) on the growth of larval American toads (Anaxyrus americanus), expressed as total length (TL) of the tadpoles, over 60 days post initial exposure to the herbicides. Measurements of growth were taken at days 0, 14, 34, 48 and 60 of the experiment. Effects of both atrazine and glyphosate on short-term growth were detected at day 14 * (P < 0.05). For longer-term growth, tadpoles were pooled across the Batrachochytrium dendrobatidis (Bd) treatments, which consisted of exposure, or not, to Bd at days 15 and 18 of the experiment, and following a highly conservative Bonferroni adjustment, 180 µg/L of atrazine significantly reduced tadpole growth until day 60 # (P < 0.0005 vs herbicide controls).
Fig. 3. Effects (LSMEANS) of exposure to Batrachochytrium dendrobatidis (Bd) on the growth of larval American toads (Anaxyrus americanus), expressed as total length (TL) of the tadpoles, over 60 days post initial exposure to different concentrations of either the herbicide (a) atrazine (Aatrex® Liquid 480), or (b) glyphosate (Vision® Silviculture Herbicide), between days 0 and 14 of the experiment. Exposure to Bd occurred at days 15 and 18 of the experiment. Measurements of growth were taken at days 0, 14, 34, 48 and 60. Tadpoles in (a) and (b) were pooled across the herbicide treatments, and significant differences in TL at specific time-points are represented by an * (P < 0.05) (significant results are listed in Table S8).
Fig. 4. Independent effects of (a) a 14-day exposure to different concentrations of the herbicide atrazine (Aatrex® Liquid 480), (b) subsequent exposure to the fungal pathogen Batrachochytrium dendrobatidis (Bd), and (c) the combined effects of these exposures, on the Gosner stages of larval development of American toads (Anaxyrus americanus), as recorded at 70 days post initial exposure to the herbicide. Significant differences in development compared to controls are represented by an * (P < 0.05).
Fig. 5. Independent effects of (a) a 14-day exposure to different concentrations of the herbicide glyphosate (Vision® Silviculture Herbicide), (b) subsequent exposure to the fungal pathogen Batrachochytrium dendrobatidis (Bd), and (c) the combined effects of these exposures, on the Gosner stages of larval development of American toads (Anaxyrus americanus), as recorded at 70 days post initial exposure to the herbicide. No significant differences in development compared to controls were found (P > 0.05).
