Photo: Kochia, southwest Montana. © 2020 Delena Norris-Tull
Impacts of Pesticides on Wildlife, other than Insects
Summaries of the research and commentary by Dr. Delena Norris-Tull, Professor Emerita of Science Education, University of Montana Western, October 2020.
Impact of Glyphosate on Birds
Recent research on the impacts of herbicides on wildlife other than insects seem to be sparse. Here are a few examples of what I did find. Each of these recent research studies includes a fairly thorough review of relevant research.
Ruuskanen, et al., 2020, reported on an experimental study of the impact of glyphosate on the embryonic development of Japanese quails, after their mother had been exposed to glyphosate-based herbicides. They found glyphosate residue in the eggs and poorer embryonic development (76% of treatment eggs showed normal development, compared to 89% in the control). In addition, embryonic brain tissue showed 20% higher lipid damage. The most concerning aspect of this study was the authors’ comment that this was the first long-term study assessing the impact of parental bird exposure to glyphosate on embryonic development.
Herbicides appear to have significantly less impact on declining bird populations than do insecticides and fungicides.
Impacts of Pesticides on Birds
Mineau & Whiteside, 2013, summarized the research on pesticide toxicity in birds. They reported that in North America, grassland birds have been declining more rapidly than other birds from other biomes. 215 species of migrant birds use North American agricultural areas. Agriculture has been linked to the decline of many species. Agricultural intensification has been considered the driving factor. But Mineau & Whiteside, 2013, conclude that perhaps the most important factor is the increased use of pesticides, particularly insecticides and fungicides. They refer to the Avian Incident Monitoring System, a joint project of the US EPA and the American Bird Conservancy, which reports that 113 pesticides have caused “direct bird mortality.” They point to a number of studies that estimate direct toxic effects of pesticides to have caused the death of tens of millions of birds per year. The removal from use of some of the more lethal pesticides, due to concerns of impacts on human health, may have already lowered the avian death rate.
Mineau & Whiteside, 2013, analyzed USDA data from the States on pesticide use (including herbicides, insecticides, and fungicides) from 1990-1998. The report focused on the mid-point data from 1992, before a number of restrictions were implemented on toxic organophosphorous insecticides. And they used data from the USGS Breeding Bird Survey to estimate bird species trends in the 45 conterminous States. They calculated the rate of each species’ decline or increase, between 1980 and 2003. They correlated bird mortality data with five predictive variables: farming intensity, lethal pesticide risk, insecticide use, herbicide use, change in permanent pasture, and change in cropped pasture. Due to the strong inter-correlations between most of these variables, they narrowed their analysis to only three variables: change in cropped pasture, change in permanent pasture, and lethal pesticide risk. They found that, “even in the full list of models with all 5 predictors, ‘lethal pesticide risk’ offered the best single-predictor model. The second best single-predictor model was with ‘insecticide use’ and ‘change in cropped pasture’ came in third place. ‘Lethal pesticide risk’ as a predictor variable was 3.9 times more plausible than ‘change in cropped pasture’ based on the evidence ratio.”
Mineau & Whiteside, 2013, stated, “Our results suggest that the use of lethally toxic insecticides cannot be ignored when trying to identify causes of grassland population declines in North America. Indeed, they offer a more plausible explanation for overall declines than does the oft-cited ‘habitat loss through agricultural intensification.’ It was remarkable that loss of permanent pasture did not appear to be much of a predictor of grassland bird declines.” Herbicides use was not a strong predictor of bird mortalities. Mineau & Whiteside, 2006, found that “only a small proportion of total cropland need be treated with a dangerous pesticide to affect overall population trends... Although pastures are believed to receive much lower insecticide loads than other crops, alfalfa still carries the third highest lethal risk of any crop based on pesticide use.”
Impacts of Herbicides on Fish
Lamb, et al., 2020, conducted an experiment in New Zealand on the use of herbicides on fish, using zebrafish, popular aquarium fish that are often used as vertebrate models in scientific experiments on drugs, etc. They report that, “Exposure to endocrine and neuroendocrine disrupting chemicals (EDCs) are reported to induce a variety of aberrant behaviors” especially when vertebrates are exposed to them in early life. “EDCs interfere with the molecular mechanisms that underpin behavior, such as gene expression, hormone levels, neurotransmitter levels, and the molecular machinery that mediates between these inputs.”
Lamb, et al., 2020, wanted to examine the impact of the herbicide atrazine across generations. They conducted experiments to examine the transmission of atrazine effects from adult male zebrafish that were exposed to atrazine during early adolescent development, to their P1 unexposed offspring. Atrazine can have a variety of neuroendocrine disrupting properties. Lamb, et al., 2020, state “to our knowledge, no study has yet explored how atrazine may affect behavioral traits of unexposed offspring.” They exposed juvenile zebrafish to several dosage levels of atrazine (0.3, 3, and 30 parts per billion) during sexual differentiation. The adult males mated with unexposed females. The F1 offspring were tested as adults. Their behaviors were assessed by exposing them to various objects in the fish tank and filming their reactions. In addition, brain tissue assays were conducted.
Lamb, et al., 2020, results:
Test 1: The F1 fish were placed in a “novel arena.” In previous studies, exposure to an unfamiliar environment after chemical exposure has been shown to increase fish anxiety, often causing them to swim to the bottom. There was no difference between treatment and control groups placed in a “novel arena,” in the amount of time spent in the bottom zone of the tanks.
Test 2: F1 fish were placed in a tank with a “novel object,” an orange rubber bung attached to fishing wire hanging in the middle of the arena. The F1 treatment fish (fish paternally exposed to 0.3ppb atrazine) spent more time at the bottom of the tank that did the control group. A slight but non-significant increase in bottom diving was experienced by the F1 treatment group, paternally exposed to 3ppb atrazine, and no significant differences occurred with the F1 treatment group, paternally exposed to 30 ppb atrazine. Male fish spent less time at the bottom zone than female fish across both tests, novel arena and novel object. “Paternal atrazine exposure significantly increased the latency to enter the top zone of the novel arena in all F1 atrazine treatment groups compared to controls.” In all treatments, male fish moved to the top zone faster than females. Male fish were far more likely to approach the novel object than females.
Test 3: “The time that F1 fish spent interacting with a mirror was significantly lower in the 0.3 ppb treatment and 30 ppb atrazine treatment compared to control.” F1 fish from the 3.0 ppb treatment had a non-significant decrease compared to the control. Male fish spent more time interacting with the mirror than did females.
Across all tests there were no differences between the groups in their exploratory behaviors. But males were more exploratory than females. “During both the novel arena and novel object test, no significant differences in activity were observed across any of the treatment groups compared to controls…[But] offspring from the 0.3 ppb and 30 ppb treatment groups travelled significantly less than offspring from control males during the mirror test… Offspring from the 3 ppb treatment also travelled less than control offspring, but this observation was marginally non-significant… Male offspring were more active than female offspring, and travelled a greater total distance” in all tests.
Brain assays: Lamb, et al., 2020, evaluated mRNA transcription within brains of the F1 fish and found significant differences within both genes that tracked with the behavioral differences, suggesting “possible serotonergic dysregulation”
Lamb, et al., 2020, conclusions: “We found that several aspects of progeny behavior were altered by paternal exposure to environmentally relevant concentrations of atrazine, thus representing intergenerational effects on behavior, though many of the effects on behavior were non dose-dependent. Moreover, some aspects of the serotonergic system were disrupted in the offspring, though given the high variation, further research is needed. Overall, these results add to the ecological consequences of environmental contaminants, most importantly, that further research may reveal that effects may be further propagated down the germline.”
Breckels & Kilgour, 2018, conducted a review of the research on the impacts of herbicides on nontarget aquatic organisms. At the time of publication, only diquat, a broad-spectrum contact herbicide used to control free-floating plants, was registered in Canada for aquatic use. Glyphosate and imazapyr have been given emergency registration status and are likely to be approved in the future. Most studies on the potential impacts to nontarget organisms are conducted in laboratory settings. It is expected that similar research conducted in the field would show less impact on nontarget organisms than in laboratory settings.
Breckels & Kilgour, 2018, reviewed related field research on all three herbicides. Their review revealed that for diquat and glyphosate there were “generally negligible or short-lived impacts on fish and aquatic invertebrates in situ.” However, “There are no field data documenting the sensitivities of fish or amphibians to aquatic formulations of imazapyr…. The [diquat] field studies that have been undertaken have been somewhat limited in number and have not considered all of the possible receiving environment conditions.”
The review of research also indicated herbicide application was often beneficial, due to the modifications it made to the habitat. However, some “surfactants used to increase herbicide efficacy have been suggested to be more toxic than the herbicide itself.” Thus they recommend that future research examine the impacts of the combination of herbicides plus surfactants.
Suzawa & Ingraham, 2008, report that, “Endocrine disrupting chemicals (EDCs) affect the reproductive health of fish and amphibious wildlife…, but their impact on mammals and particularly humans is less clear…. Numerous studies in fish, amphibians, reptiles and mammals all suggest that ATR [atrazine] can alter normal endocrine, neuroendocrine and immune responses…. We used mammalian cell lines and zebrafish as model systems to address the in vivo and in vitro roles of ATR in activating aromatase expression…. To determine whether ATR and other endocrine disruptors might affect NR5A receptor activity in vivo, sexually immature zebrafish larvae were exposed to different chemicals for their potential to regulate zcyp19a1.”
Suzawa & Ingraham, 2008, results with fish: “Using quantitative PCR (qPCR) we found robust increases in expression of zcyp19a1, but not zcyp19a2 after acute exposure to ATR… in 17 days post fertilization…zebrafish... As shown previously…, estradiol…, the phyto-estrogen, genistein, and the industrial chemical bisphenol A, all elevated the relative expression of zcyp19a2 after 3 days of exposure… Significant increases in endogenous aromatase expression are observed at ecologically relevant levels of this compound.” Chronic exposure to the herbicide for six months resulted in “a dose-dependent increase in the number of female fish…with a corresponding drop in the male fish after ATR exposure when compared to the control tank.”
Suzawa & Ingraham, 2008, results with mammalian cells: Read the research report for details of the genetic testing. “The fact that ATR upregulates several peptide hormones and steroidogenic genes in mammalian cells suggests that the in vivo effects of these triazine herbicides will be much broader, extending well beyond estrogen metabolism….These findings suggest that further research is needed to determine whether high and/or chronic exposure to ATR in humans compromise normal fertility and contribute to reproductive diseases.”
Suzawa & Ingraham, 2008, conclusion: “We propose that this pervasive and persistent environmental chemical alters hormone networks…, to potentially disrupt normal endocrine development and function in lower and higher vertebrates…. Our in vivo and in vitro analyses of ATR strongly suggest that this widely used herbicide affects hormone signaling and endocrine transcriptional networks in fish and in mammalian cells. Indeed, we found that acute and chronic exposure to ATR significantly increased the endogenous levels of zcyp19a1 encoding gonadal aromatase and altered the normal sex ratio in environmental conditions in a relevant vertebrate model system. Moreover, our cellular data illustrate that ATR induces a cluster of endocrine-related genes... Endocrine-related cell types with a capacity for steroidogenesis appear to be especially sensitive to ATR, as demonstrated by the exquisite cellular specificity of the ATR response.”
References:
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Impacts of Pesticides on Wildlife, other than Insects
Summaries of the research and commentary by Dr. Delena Norris-Tull, Professor Emerita of Science Education, University of Montana Western, October 2020.
Impact of Glyphosate on Birds
Recent research on the impacts of herbicides on wildlife other than insects seem to be sparse. Here are a few examples of what I did find. Each of these recent research studies includes a fairly thorough review of relevant research.
Ruuskanen, et al., 2020, reported on an experimental study of the impact of glyphosate on the embryonic development of Japanese quails, after their mother had been exposed to glyphosate-based herbicides. They found glyphosate residue in the eggs and poorer embryonic development (76% of treatment eggs showed normal development, compared to 89% in the control). In addition, embryonic brain tissue showed 20% higher lipid damage. The most concerning aspect of this study was the authors’ comment that this was the first long-term study assessing the impact of parental bird exposure to glyphosate on embryonic development.
Herbicides appear to have significantly less impact on declining bird populations than do insecticides and fungicides.
Impacts of Pesticides on Birds
Mineau & Whiteside, 2013, summarized the research on pesticide toxicity in birds. They reported that in North America, grassland birds have been declining more rapidly than other birds from other biomes. 215 species of migrant birds use North American agricultural areas. Agriculture has been linked to the decline of many species. Agricultural intensification has been considered the driving factor. But Mineau & Whiteside, 2013, conclude that perhaps the most important factor is the increased use of pesticides, particularly insecticides and fungicides. They refer to the Avian Incident Monitoring System, a joint project of the US EPA and the American Bird Conservancy, which reports that 113 pesticides have caused “direct bird mortality.” They point to a number of studies that estimate direct toxic effects of pesticides to have caused the death of tens of millions of birds per year. The removal from use of some of the more lethal pesticides, due to concerns of impacts on human health, may have already lowered the avian death rate.
Mineau & Whiteside, 2013, analyzed USDA data from the States on pesticide use (including herbicides, insecticides, and fungicides) from 1990-1998. The report focused on the mid-point data from 1992, before a number of restrictions were implemented on toxic organophosphorous insecticides. And they used data from the USGS Breeding Bird Survey to estimate bird species trends in the 45 conterminous States. They calculated the rate of each species’ decline or increase, between 1980 and 2003. They correlated bird mortality data with five predictive variables: farming intensity, lethal pesticide risk, insecticide use, herbicide use, change in permanent pasture, and change in cropped pasture. Due to the strong inter-correlations between most of these variables, they narrowed their analysis to only three variables: change in cropped pasture, change in permanent pasture, and lethal pesticide risk. They found that, “even in the full list of models with all 5 predictors, ‘lethal pesticide risk’ offered the best single-predictor model. The second best single-predictor model was with ‘insecticide use’ and ‘change in cropped pasture’ came in third place. ‘Lethal pesticide risk’ as a predictor variable was 3.9 times more plausible than ‘change in cropped pasture’ based on the evidence ratio.”
Mineau & Whiteside, 2013, stated, “Our results suggest that the use of lethally toxic insecticides cannot be ignored when trying to identify causes of grassland population declines in North America. Indeed, they offer a more plausible explanation for overall declines than does the oft-cited ‘habitat loss through agricultural intensification.’ It was remarkable that loss of permanent pasture did not appear to be much of a predictor of grassland bird declines.” Herbicides use was not a strong predictor of bird mortalities. Mineau & Whiteside, 2006, found that “only a small proportion of total cropland need be treated with a dangerous pesticide to affect overall population trends... Although pastures are believed to receive much lower insecticide loads than other crops, alfalfa still carries the third highest lethal risk of any crop based on pesticide use.”
Impacts of Herbicides on Fish
Lamb, et al., 2020, conducted an experiment in New Zealand on the use of herbicides on fish, using zebrafish, popular aquarium fish that are often used as vertebrate models in scientific experiments on drugs, etc. They report that, “Exposure to endocrine and neuroendocrine disrupting chemicals (EDCs) are reported to induce a variety of aberrant behaviors” especially when vertebrates are exposed to them in early life. “EDCs interfere with the molecular mechanisms that underpin behavior, such as gene expression, hormone levels, neurotransmitter levels, and the molecular machinery that mediates between these inputs.”
Lamb, et al., 2020, wanted to examine the impact of the herbicide atrazine across generations. They conducted experiments to examine the transmission of atrazine effects from adult male zebrafish that were exposed to atrazine during early adolescent development, to their P1 unexposed offspring. Atrazine can have a variety of neuroendocrine disrupting properties. Lamb, et al., 2020, state “to our knowledge, no study has yet explored how atrazine may affect behavioral traits of unexposed offspring.” They exposed juvenile zebrafish to several dosage levels of atrazine (0.3, 3, and 30 parts per billion) during sexual differentiation. The adult males mated with unexposed females. The F1 offspring were tested as adults. Their behaviors were assessed by exposing them to various objects in the fish tank and filming their reactions. In addition, brain tissue assays were conducted.
Lamb, et al., 2020, results:
Test 1: The F1 fish were placed in a “novel arena.” In previous studies, exposure to an unfamiliar environment after chemical exposure has been shown to increase fish anxiety, often causing them to swim to the bottom. There was no difference between treatment and control groups placed in a “novel arena,” in the amount of time spent in the bottom zone of the tanks.
Test 2: F1 fish were placed in a tank with a “novel object,” an orange rubber bung attached to fishing wire hanging in the middle of the arena. The F1 treatment fish (fish paternally exposed to 0.3ppb atrazine) spent more time at the bottom of the tank that did the control group. A slight but non-significant increase in bottom diving was experienced by the F1 treatment group, paternally exposed to 3ppb atrazine, and no significant differences occurred with the F1 treatment group, paternally exposed to 30 ppb atrazine. Male fish spent less time at the bottom zone than female fish across both tests, novel arena and novel object. “Paternal atrazine exposure significantly increased the latency to enter the top zone of the novel arena in all F1 atrazine treatment groups compared to controls.” In all treatments, male fish moved to the top zone faster than females. Male fish were far more likely to approach the novel object than females.
Test 3: “The time that F1 fish spent interacting with a mirror was significantly lower in the 0.3 ppb treatment and 30 ppb atrazine treatment compared to control.” F1 fish from the 3.0 ppb treatment had a non-significant decrease compared to the control. Male fish spent more time interacting with the mirror than did females.
Across all tests there were no differences between the groups in their exploratory behaviors. But males were more exploratory than females. “During both the novel arena and novel object test, no significant differences in activity were observed across any of the treatment groups compared to controls…[But] offspring from the 0.3 ppb and 30 ppb treatment groups travelled significantly less than offspring from control males during the mirror test… Offspring from the 3 ppb treatment also travelled less than control offspring, but this observation was marginally non-significant… Male offspring were more active than female offspring, and travelled a greater total distance” in all tests.
Brain assays: Lamb, et al., 2020, evaluated mRNA transcription within brains of the F1 fish and found significant differences within both genes that tracked with the behavioral differences, suggesting “possible serotonergic dysregulation”
Lamb, et al., 2020, conclusions: “We found that several aspects of progeny behavior were altered by paternal exposure to environmentally relevant concentrations of atrazine, thus representing intergenerational effects on behavior, though many of the effects on behavior were non dose-dependent. Moreover, some aspects of the serotonergic system were disrupted in the offspring, though given the high variation, further research is needed. Overall, these results add to the ecological consequences of environmental contaminants, most importantly, that further research may reveal that effects may be further propagated down the germline.”
Breckels & Kilgour, 2018, conducted a review of the research on the impacts of herbicides on nontarget aquatic organisms. At the time of publication, only diquat, a broad-spectrum contact herbicide used to control free-floating plants, was registered in Canada for aquatic use. Glyphosate and imazapyr have been given emergency registration status and are likely to be approved in the future. Most studies on the potential impacts to nontarget organisms are conducted in laboratory settings. It is expected that similar research conducted in the field would show less impact on nontarget organisms than in laboratory settings.
Breckels & Kilgour, 2018, reviewed related field research on all three herbicides. Their review revealed that for diquat and glyphosate there were “generally negligible or short-lived impacts on fish and aquatic invertebrates in situ.” However, “There are no field data documenting the sensitivities of fish or amphibians to aquatic formulations of imazapyr…. The [diquat] field studies that have been undertaken have been somewhat limited in number and have not considered all of the possible receiving environment conditions.”
The review of research also indicated herbicide application was often beneficial, due to the modifications it made to the habitat. However, some “surfactants used to increase herbicide efficacy have been suggested to be more toxic than the herbicide itself.” Thus they recommend that future research examine the impacts of the combination of herbicides plus surfactants.
Suzawa & Ingraham, 2008, report that, “Endocrine disrupting chemicals (EDCs) affect the reproductive health of fish and amphibious wildlife…, but their impact on mammals and particularly humans is less clear…. Numerous studies in fish, amphibians, reptiles and mammals all suggest that ATR [atrazine] can alter normal endocrine, neuroendocrine and immune responses…. We used mammalian cell lines and zebrafish as model systems to address the in vivo and in vitro roles of ATR in activating aromatase expression…. To determine whether ATR and other endocrine disruptors might affect NR5A receptor activity in vivo, sexually immature zebrafish larvae were exposed to different chemicals for their potential to regulate zcyp19a1.”
Suzawa & Ingraham, 2008, results with fish: “Using quantitative PCR (qPCR) we found robust increases in expression of zcyp19a1, but not zcyp19a2 after acute exposure to ATR… in 17 days post fertilization…zebrafish... As shown previously…, estradiol…, the phyto-estrogen, genistein, and the industrial chemical bisphenol A, all elevated the relative expression of zcyp19a2 after 3 days of exposure… Significant increases in endogenous aromatase expression are observed at ecologically relevant levels of this compound.” Chronic exposure to the herbicide for six months resulted in “a dose-dependent increase in the number of female fish…with a corresponding drop in the male fish after ATR exposure when compared to the control tank.”
Suzawa & Ingraham, 2008, results with mammalian cells: Read the research report for details of the genetic testing. “The fact that ATR upregulates several peptide hormones and steroidogenic genes in mammalian cells suggests that the in vivo effects of these triazine herbicides will be much broader, extending well beyond estrogen metabolism….These findings suggest that further research is needed to determine whether high and/or chronic exposure to ATR in humans compromise normal fertility and contribute to reproductive diseases.”
Suzawa & Ingraham, 2008, conclusion: “We propose that this pervasive and persistent environmental chemical alters hormone networks…, to potentially disrupt normal endocrine development and function in lower and higher vertebrates…. Our in vivo and in vitro analyses of ATR strongly suggest that this widely used herbicide affects hormone signaling and endocrine transcriptional networks in fish and in mammalian cells. Indeed, we found that acute and chronic exposure to ATR significantly increased the endogenous levels of zcyp19a1 encoding gonadal aromatase and altered the normal sex ratio in environmental conditions in a relevant vertebrate model system. Moreover, our cellular data illustrate that ATR induces a cluster of endocrine-related genes... Endocrine-related cell types with a capacity for steroidogenesis appear to be especially sensitive to ATR, as demonstrated by the exquisite cellular specificity of the ATR response.”
References:
- Breckels, R.D., & Kilgour, B.W. (2018). Aquatic herbicide applications for the control of aquatic plants in Canada: Effects to nontarget aquatic organisms. Environmental Reviews, 26(3):333-338.
- Lamb, S.D., Chia, J.H.Z., Johnson, S.L. (April 10, 2020). Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring. PLos ONE, 15(4): e0228357. https://doi.org/10.1371/journal.pone.0228357
- Mineau, P., & Whiteside, M. (Feb. 20, 2013). Pesticide acute toxicity is a better correlate of U.S. grassland bird declines than agricultural intensification. PLS ONE, 8(2):e57457. doi: 10.1371/journal.pone.0057457
- Ruuskanen, S., Rainio, M.J., Uusitalo, M., Saikkonen, K., & Helander, M. (April 14, 2020). Effects of parental exposure to glyphosate-based herbicides on embryonic development and oxidative status: A long-term experiment in a bird model. Scientific Reports, 10(1): 1-7.
- Suzawa, M., & Ingraham, H.A. (May 1, 2008). The herbicide atrazine activates endocrine gene networks via non-steroidal NR5A nuclear receptors in fish and mammalian cells. PLos ONE, 3(5): e2117. doi:10.1371/journal.pone.0002117
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