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Pollinators

Impact of Pesticides on Pollinators

The science has become increasingly clear that pesticides, either acting individually or synergistically, play a critical role in the ongoing decline of honey bees and wild pollinators. Some pesticides produce sublethal effects in honeybees, which include disruptions in mobility, navigation, and feeding behavior. Decreased foraging activity, along with olfactory learning performance and decreased hive activity has also been observed. Other pollinators, such as the monarch butterfly, are indirectly affected by pesticides through habitat destruction brought on by the proliferation of genetically engineered (GE) crops and mono-crop agriculture. Part of the decline of monarch butterflies stems from the loss of milkweed, a native plant where the butterflies lay their eggs and is their main food source.

  • In 2015, researchers found that bumblebees exposed to field levels of neonicotinoids accumulate the toxic pesticides in their brains. Acute and chronic exposure increased neuronal vulnerability to mitochondrial dysfunction.
  • Another recent study provided supporting evidence to previous work showing that sublethal doses of imidicloprid, a toxic neonicotinoid insecticide, impairs olfactory learning in exposed honey bee workers. The study found that:
      • “Adults that ingested a single imidacloprid dose as low as 0.1 ng/bee had significantly reduced olfactory learning acquisition, which was 1.6-fold higher in control bees.”
      • “Bees exposed as larvae to a total dose of 0.24 ng/bee had significantly impaired olfactory learning when tested as adults; control bees exhibited up to 4.8-fold better short-term learning acquisition.”
  • In 2014, researches used Radio-Frequency Identification (RFID) tagging technology to examine how the day-to-day foraging patterns of bumblebees were affected when exposed to either a neonicotinoid (imidacloprid) and/or a
    Monarch Butterfly on Milkweed
    Monarch Butterfly on Milkweed. Photo by Lee Ruk. 
    pyrethroid (λ-cyhalothrin) independently and in combination over a four-week period. They found that neonicotinoid exposure has both acute and chronic effects on overall foraging activity; the performance of bees exposed to imidacloprid became worse, resulting in chronic behavioral impairment.
  • A recent study on monarchs attributed the disappearance of milkweed plants primarily to the use of GE corn and soybean crops. Scientists also point to the prolific use of herbicides in the Midwest eliminating these plants, and found that 70% of the losses of milkweed between 1995 and 2013 were located in agricultural areas.

[See More Scientific Studies Below]

For more details about the impact of pesticides on pollinators, see Beyond Pesticides’ BEE Protective page.

Economic Cost

In a 2009 study by Gallai et. al., the total economic value of pollinators globally was estimated to be $153 billion per year. Estimates vary for the United States as time moves forward, but regardless of the differing economic figures, the impacts of insecticides used on agriculture to bees and other pollinators are vast. In a 2005 study by David Pimentel, it was estimated that 5% of US honey bee colonies are killed due to pesticide exposure, leading to a $13.3 million annual loss. Honey and wax losses total to about $25.3 million a year. Pimentel speculated that due to the fact that 4-6 million hectares of land are heavily treated with pesticides, beekeepers cannot use what would otherwise be considered suitable apiary land. This yearly loss in potential honey production totals about $27 million. In addition to these losses, many crops fail due to lack of pollination. He estimated that these annual pollination losses caused by pesticides could be as high as $210 million. Pimental’s estimates are conservative, considering they were made before the advent of colony collapse disorder (CCD), and before large-scale pollinator losses began. In 2006, Losey and Vaughan estimated that native pollinators are responsible for $3.07 billion of fruit and vegetable production in the US. Then, in 2012, N.W. Calderone estimated that in 2009, the economic value of crops dependent on pollinators was approximately $15.12 billion for the US.

Litigation & Lawsuits

Beyond Pesticides, concerned citizens, and other environmental organizations filed a civil action suit against EPA in March 2013 for using clothianidin and thiamethoxam, two pesticides classified as neonicotinoids. The lawsuit aims to hold EPA accountable for the violation of Federal Insecticide, Fungicide and Rodenticide Act (FIFRA), the Endangered Species Act (ESA) and the Administrative Procedure Act (APA). EPA has approved the use of these pesticides without notification to the Federal Register, and without a public comment period, which violates FIFRA and the APA.

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Honeybees
Honeybees. Photo by Paul Rollings. 

In July 2013, several beekeeping organizations filed suit against the U.S. Environmental Protection Agency’s (EPA) to reverse a recent decision to register a new pesticide, sulfoxaflor, which is highly toxic to bees. This chemical is also considered by some scientists to be in the same class as neonicotinoids due to the fact that it has the same mode of action, although industry refuses to consider this claim, In December 2013, environmental and farm groups, including Beyond Pesticides, came together to file a legal brief in support of the nation’s major beekeeping associations’ lawsuit against the EPA. In March 2015, the 9th U.S. Circuit Court of Appeals agreed to hear the case.

 

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In March 2015, a federal court ruled against the use of neonicotinoid insecticides linked with destruction of bee colonies and other beneficial insects in national wildlife refuges in the Midwest region. The ruling capped a legal campaign to end the planting of genetically engineered (GE) crops and other industrial agricultural practices on national wildlife refuges across the country. In July 2014, FWS decided that it will phase out the use of GE crops to feed wildlife and ban neonicotinoid insecticides from all wildlife refuges nationwide by January 2016. This new policy still allows for case-by-case exceptions.

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What Can You Do?

A necessary first step is to avoid using toxic pesticides in and around your home, and encourage others to do the same. For other helpful tips, see Beyond Pesticides’ webpage on Managing Landscapes with Pollinators in Mind. Concerned residents can find more ways to take action in their community through the BEE Protective webpage.

Scientific Studies: 

  • A contemporary survey of bumble bee diversity across the state of California.
    Bumble bees (genus Bombus) are important pollinators with more than 260 spe -cies found worldwide, many of which are in decline. Twenty-five species occur in California with the highest species abundance and diversity found in coastal, north -ern, and montane regions. No recent studies have examined California bumble bee di -versity across large spatial scales nor explored contemporary community composition patterns across the state. To fill these gaps, we collected 1740 bumble bee individuals, representing 17 species from 17 sites (~100 bees per site) in California, using an as -semblage monitoring framework. This framework is intended to provide an accurate estimate of relative abundance of more common species without negatively impact -ing populations through overcollection. Our sites were distributed across six ecore -gions, with an emphasis on those that historically hosted high bumble bee diversity. We compared bumble bee composition among these sites to provide a snapshot of California bumble bee biodiversity in a single year. Overall, the assemblage monitor-ing framework that we employed successfully captured estimated relative abundance of species for most sites, but not all. This shortcoming suggests that bumble bee biodiversity monitoring in California might require multiple monitoring approaches, including greater depth of sampling in some regions, given the variable patterns in bumble bee abundance and richness throughout the state. Our study sheds light on the current status of bumble bee diversity in California, identifies some areas where greater sampling effort and conservation action should be focused in the future, and performs the first assessment of an assembly monitoring framework for bumble bee communities in the state.
    [Fisher, K., Watrous, K.M., Williams, N.M., Richardson, L.L. and Woodard, S.H. Ecology and Evolution, 12(3), p.e8505.]
  • Acaricide flumethrin-induced sublethal risks in honeybees are associated with gut symbiotic bacterium Gilliamella apicola through microbe-host metabolic interactions
    Flumethrin is one of the few acaricides that permit the control of Varroa disease or varroosis in bee colonies. However, flumethrin accumulates in hive products. We previously discovered that sublethal doses of flumethrin induce significant physiological stress in honeybees (Apis mellifera L.), however its potential impacts on the honeybee gut microenvironment remains unknown. To fill this gap, honeybees were exposed to a field-relevant concentration of flumethrin (10 μg/L) for 14 d and its potential impacts on gut system were evaluated. The results indicated that flumethrin triggered immune responses in the gut but had limited effects on survival and gut microbial composition. However, survival stress drastically increased in bees exposed to antibiotics, suggesting that the gut microbiota is closely related to flumethrin-induced dysbiosis in the bee gut. Based on a non-targeted metabolomics approach, flumethrin at 10 μg/L considerably altered the composition of intestinal metabolites, and we discovered that this metabolic stress was closely linked with a reduction of gut core bacterial endosymbiont Gilliamella spp. through a combination of microbiological and metabolomics investigations. Finally, an in vitro study showed that while flumethrin does not directly inhibit the growth of Gilliamella apicola isolates, it does have a significant impact on the glycerophospholipid metabolism in bacteria cells, which was also observed in host bees. These findings indicated that even though flumethrin administered at environmental relevant concentrations does not significantly induce death in honeybees, it still alters the metabolism balance between honeybees and the gut symbiotic bacterium, G. apicola. The considerable negative impact of flumethrin on the honeybee gut microenvironment emphasizes the importance of properly monitoring acaricide to avoid potential environmental concerns, and further studies are needed to illustrate the mode of action of bee health-gut microbiota-exogenous pesticides.
    [Qi, S., Al Naggar, Y., Li, J., Liu, Z., Xue, X., Wu, L., El-Seedi, H.R. and Wang, K., 2022. Chemosphere, 307, p.136030.]
  • Bees under interactive stressors: the novel insecticides flupyradifurone and sulfoxaflor along with the fungicide azoxystrobin disrupt the gut microbiota of honey bees and increase opportunistic bacterial pathogens
    The gut microbiome plays an important role in bee health and disease. But it can be disrupted by pesticides and in-hive chemicals, putting honey bee health in danger. We used a controlled and fully crossed laboratory experimental design to test the effects of a 10-day period of chronic exposure to field-realistic sublethal concentrations of two nicotinic acetylcholine receptor agonist insecticides (nACHRs), namely flupyradifurone (FPF) and sulfoxaflor (Sulf), and a fungicide, azoxystrobin (Azoxy), individually and in combination, on the survival of individual honey bee workers and the composition of their gut microbiota (fungal and bacterial diversity). Metabarcoding was used to examine the gut microbiota on days 0, 5, and 10 of pesticide exposure to determine how the microbial response varies over time; to do so, the fungal ITS2 fragment and the V4 region of the bacterial 16S rRNA were targeted. We found that FPF has a negative impact on honey bee survival, but interactive (additive or synergistic) effects between either insecticide and the fungicide on honey bee survival were not statistically significant. Pesticide treatments significantly impacted the microbial community composition. The fungicide Azoxy substantially reduced the Shannon diversity of fungi after chronic exposure for 10 days. The relative abundance of the top 10 genera of the bee gut microbiota was also differentially affected by the fungicide, insecticides, and fungicide-insecticide combinations. Gut microbiota dysbiosis was associated with an increase in the relative abundance of opportunistic pathogens such as Serratia spp. (e.g. S. marcescens), which can have devastating consequences for host health such as increased susceptibility to infection and reduced lifespan. Our findings raise concerns about the long-term impact of novel nACHR insecticides, particularly FPF, on pollinator health and recommend a novel methodology for a refined risk assessment that includes the potential effects of agrochemicals on the gut microbiome of bees.

    The gut microbiome plays an important role in bee health and disease. But it can be disrupted by pesticides and in-hive chemicals, putting honey bee health in danger. We used a controlled and fully crossed laboratory experimental design to test the effects of a 10-day period of chronic exposure to field-realistic sublethal concentrations of two nicotinic acetylcholine receptor agonist insecticides (nACHRs), namely flupyradifurone (FPF) and sulfoxaflor (Sulf), and a fungicideazoxystrobin (Azoxy), individually and in combination, on the survival of individual honey bee workers and the composition of their gut microbiota (fungal and bacterial diversity). Metabarcoding was used to examine the gut microbiota on days 0, 5, and 10 of pesticide exposure to determine how the microbial response varies over time; to do so, the fungal ITS2 fragment and the V4 region of the bacterial 16S rRNA were targeted. We found that FPF has a negative impact on honey bee survival, but interactive (additive or synergistic) effects between either insecticide and the fungicide on honey bee survival were not statistically significant. Pesticide treatments significantly impacted the microbial community composition. The fungicide Azoxy substantially reduced the Shannon diversity of fungi after chronic exposure for 10 days. The relative abundance of the top 10 genera of the bee gut microbiota was also differentially affected by the fungicide, insecticides, and fungicide-insecticide combinations. Gut microbiota dysbiosis was associated with an increase in the relative abundance of opportunistic pathogens such as Serratia spp. (e.g. S. marcescens), which can have devastating consequences for host health such as increased susceptibility to infection and reduced lifespan. Our findings raise concerns about the long-term impact of novel nACHR insecticides, particularly FPF, on pollinator health and recommend a novel methodology for a refined risk assessment that includes the potential effects of agrochemicals on the gut microbiome of bees.
    [Al Naggar, Y., Singavarapu, B., Paxton, R.J. and Wubet, T., 2022. Science of The Total Environment, 849, p.157941.]

  • Glyphosate impairs collective thermoregulation in bumblebees.
    Insects are facing a multitude of anthropogenic stressors, and the recent decline in their biodiversity is threatening ecosystems and economies across the globe. We investigated the impact of glyphosate, the most commonly used herbicide worldwide, on bumblebees. Bumblebee colonies maintain their brood at high temperatures via active thermogenesis, a prerequisite for colony growth and reproduction. Using a within-colony comparative approach to examine the effects of long-term glyphosate exposure on both individual and collective thermoregulation, we found that whereas effects are weak at the level of the individual, the collective ability to maintain the necessary high brood temperatures is decreased by more than 25% during periods of resource limitation. For pollinators in our heavily stressed ecosystems, glyphosate exposure carries hidden costs that have so far been largely overlooked.
    [Weidenmüller, A., Meltzer, A., Neupert, S., Schwarz, A. and Kleineidam, C. Science, 376(6597), pp.1122-1126.]
  • Herbicide spray drift from ground and aerial applications: Implications for potential pollinator foraging sources
    A field spray drift experiment using florpyrauxifen-benzyl was conducted to measure drift from commercial ground and aerial applications, evaluate soybean [Glycine max (L.) Merr.] impacts, and compare to United States Environmental Protection Agency (US EPA) drift models. Collected field data were consistent with US EPA model predictions. Generally, with both systems applying a Coarse spray in a 13-kph average wind speed, the aerial application had a 5.0- to 8.6-fold increase in drift compared to the ground application, and subsequently, a 1.7- to 3.6-fold increase in downwind soybean injury. Soybean reproductive structures were severely reduced following herbicide exposure, potentially negatively impacting pollinator foraging sources. Approximately a 25% reduction of reproductive structures up to 30.5-m downwind and nearly a 100% reduction at 61-m downwind were observed for ground and aerial applications, respectively. Aerial applications would require three to five swath width adjustments upwind to reduce drift potential similar to ground applications.
    [Butts, T.R., Fritz, B.K., Kouame, K., Norsworthy, J.K., Barber, L.T., Ross, W.J., Lorenz, G.M., Thrash, B.C., Bateman, N.R. and Adamczyk, J.J., 2022. Scientific Reports, 12(1), pp.1-15.]
  • Pesticide-induced disturbances of bee gut microbiotas.
    Social bee gut microbiotas play key roles in host health and performance. Worryingly, a growing body of literature shows that pesticide exposure can disturb these microbiotas. Most studies examine changes in taxonomic composition in Western honey bee (Apis mellifera) gut microbiotas caused by insecticide exposure. Core bee gut microbiota taxa shift in abundance after exposure but are rarely eliminated, with declines in Bifidobacteriales and Lactobacillus near melliventris abundance being the most common shifts. Pesticide concentration, exposure duration, season and concurrent stressors all influence whether and how bee gut microbiotas are disturbed. Also, the mechanism of disturbance—i.e. whether a pesticide directly affects microbial growth or indirectly affects the microbiota by altering host health—likely affects disturbance consistency. Despite growing interest in this topic, important questions remain unanswered. Specifically, metabolic shifts in bee gut microbiotas remain largely uninvestigated, as do effects of pesticide-disturbed gut microbiotas on bee host performance. Furthermore, few bee species have been studied other than A. mellifera, and few herbicides and fungicides have been examined. We call for these knowledge gaps to be addressed so that we may obtain a comprehensive picture of how pesticides alter bee gut microbiotas, and of the functional consequences of these changes.
    [Hotchkiss, M.Z., Poulain, A.J. and Forrest, J.R. FEMS Microbiology Reviews, 46(2), p.fuab056.]
  • Putting pesticides on the map for pollinator research and conservation
    Wild and managed pollinators are essential to food production and the function of natural ecosystems; however, their populations are threatened by multiple stressors including pesticide use. Because pollinator species can travel hundreds to thousands of meters to forage, recent research has stressed the importance of evaluating pollinator decline at the landscape scale. However, scientists’ and conservationists’ ability to do this has been limited by a lack of accessible data on pesticide use at relevant spatial scales and in toxicological units meaningful to pollinators. Here, we synthesize information from several large, publicly available datasets on pesticide use patterns, land use, and toxicity to generate novel datasets describing pesticide use by active ingredient (kg, 1997–2017) and aggregate insecticide load (kg and honey bee lethal doses, 1997–2014) for state-crop combinations in the contiguous U.S. Furthermore, by linking pesticide datasets with land-use data, we describe a method to map pesticide indicators at spatial scales relevant to pollinator research and conservation.
    [Douglas, M.R., Baisley, P., Soba, S., Kammerer, M., Lonsdorf, E.V. and Grozinger, C.M., 2022. Scientific Data, 9(1), pp.1-15.]
  • Turnover in floral composition explains species diversity and temporal stability in the nectar supply of urban residential gardens
    Residential gardens are a valuable habitat for insect pollinators worldwide, but differences in individual gardening practices substantially affect their floral composition. It is important to understand how the floral resource supply of gardens varies in both space and time so we can develop evidence-based management recommendations to support pollinator conservation in towns and cities.
    We surveyed 59 residential gardens in the city of Bristol, UK, at monthly intervals from March to October. For each of 472 garden surveys, we combined floral abundances with nectar sugar data to quantify the nectar production of each garden, investigating the magnitude, temporal stability, and diversity and composition of garden nectar supplies.
    We found that individual gardens differ markedly in the quantity of nectar sugar they supply (from 2 to 1,662 g), and nectar production is higher in more affluent neighbourhoods, but not in larger gardens. Nectar supply peaks in July (mid-summer), when more plant taxa are in flower, but temporal patterns vary among individual gardens. At larger spatial scales, temporal variability averages out through the portfolio effect, meaning insect pollinators foraging across many gardens in urban landscapes have access to a relatively stable and continuous supply of nectar through the year.
    Turnover in species composition among gardens leads to an extremely high overall plant richness, with 636 taxa recorded flowering. The nectar supply is dominated by non-natives, which provide 91% of all nectar sugar, while shrubs are the main plant life form contributing to nectar production (58%). Two-thirds of nectar sugar is only available to relatively specialised pollinators, leaving just one-third that is accessible to all.
    Synthesis and applications. By measuring nectar supply in residential gardens, our study demonstrates that pollinator-friendly management, affecting garden quality, is more important than the size of a garden, giving every gardener an opportunity to contribute to pollinator conservation in urban areas. For gardeners interested in increasing the value of their land to foraging pollinators, we recommend planting nectar-rich shrubs with complementary flowering periods and prioritising flowers with an open structure in late summer and autumn.
    [Tew, N.E., Baldock, K.C., Vaughan, I.P., Bird, S. and Memmott, J. Journal of Applied Ecology, 59(3), pp.801-811.]
  • Co-formulant in a commercial fungicide product causes lethal and sub-lethal effects in bumble bees
    Pollinators, particularly wild bees, are suffering declines across the globe, and pesticides are thought to be drivers of these declines. Research into, and regulation of pesticides has focused on the active ingredients, and their impact on bee health. In contrast, the additional components in pesticide formulations have been overlooked as potential threats. By testing an acute oral dose of the fungicide product Amistar, and equivalent doses of each individual co-formulant, we were able to measure the toxicity of the formulation and identify the ingredient responsible. We found that a co-formulant, alcohol ethoxylates, caused a range of damage to bumble bee health. Exposure to alcohol ethoxylates caused 30% mortality and a range of sublethal effects. Alcohol ethoxylates treated bees consumed half as much sucrose as negative control bees over the course of the experiment and lost weight. Alcohol ethoxylates treated bees had significant melanisation of their midguts, evidence of gut damage. We suggest that this gut damage explains the reduction in appetite, weight loss and mortality, with bees dying from energy depletion. Our results demonstrate that sublethal impacts of pesticide formulations need to be considered during regulatory consideration, and that co-formulants can be more toxic than active ingredients.
    [Straw, E.A. and Brown, M.J. Scientific reports, 11(1), pp.1-10.]
  • Past insecticide exposure reduces bee reproduction and population growth rate
    Pesticides are linked to global insect declines, with impacts on biodiversity and essential ecosystem services. In addition to well-documented direct impacts of pesticides at the current stage or time, potential delayed “carryover” effects from past exposure at a different life stage may augment impacts on individuals and populations. We investigated the effects of current exposure and the carryover effects of past insecticide exposure on the individual vital rates and population growth of the solitary bee, Osmia lignaria. Bees in flight cages freely foraged on wildflowers, some treated with the common insecticide, imidacloprid, in a fully crossed design over 2 y, with insecticide exposure or no exposure in each year. Insecticide exposure directly to foraging adults and via carryover effects from past exposure reduced reproduction. Repeated exposure across 2 y additively impaired individual performance, leading to a nearly fourfold reduction in bee population growth. Exposure to even a single insecticide application can have persistent effects on vital rates and can reduce population growth for multiple generations. Carryover effects had profound implications for population persistence and must be considered in risk assessment, conservation, and management decisions for pollinators to mitigate the effects of insecticide exposure.
    [Stuligross, C. and Williams, N.M. Proceedings of the National Academy of Sciences, 118(48).]
  • Assessing Field‐Scale Risks of Foliar Insecticide Applications to Monarch Butterfly (Danaus plexippus) Larvae
    Establishment and maintenance of milkweed plants (Asclepias spp.) in agricultural landscapes of the north central United States are needed to reverse the decline of North America's eastern monarch butterfly (Danaus plexippus) population. Because of a lack of toxicity data, it is unclear how insecticide use may reduce monarch productivity when milkweed habitat is placed near maize and soybean fields. To assess the potential effects of foliar insecticides, acute cuticular and dietary toxicity of 5 representative active ingredients were determined: beta‐cyfluthrin (pyrethroid), chlorantraniliprole (anthranilic diamide), chlorpyrifos (organophosphate), and imidacloprid and thiamethoxam (neonicotinoids). Cuticular median lethal dose values for first instars ranged from 9.2 × 10–3 to 79 μg/g larvae for beta‐cyfluthrin and chlorpyrifos, respectively. Dietary median lethal concentration values for second instars ranged from 8.3 × 10–3 to 8.4 μg/g milkweed leaf for chlorantraniliprole and chlorpyrifos, respectively. To estimate larval mortality rates downwind from treated fields, modeled insecticide exposures to larvae and milkweed leaves were compared to dose–response curves obtained from bioassays with first‐, second‐, third‐, and fifth‐instar larvae. For aerial applications to manage soybean aphids, mortality rates at 60 m downwind were highest for beta‐cyfluthrin and chlorantraniliprole following cuticular and dietary exposure, respectively, and lowest for thiamethoxam. To estimate landscape‐scale risks, field‐scale mortality rates must be considered in the context of spatial and temporal patterns of insecticide use.
    [Krishnan, N., Zhang, Y., Bidne, K.G., Hellmich, R.L., Coats, J.R. and Bradbury, S.P., 2020. Environmental Toxicology and Chemistry, 39(4), pp.923-941.]
  • Micronucleus Test Reveals Genotoxic Effects in Bats Associated with Agricultural Activity
    Bats play a vital role in our ecosystems and economies as natural pest‐control agents, seed dispersers, and pollinators. Agricultural intensification, however, can impact bats foraging near crops, affecting the ecosystem services they provide. Exposure to pesticides, for example, may induce chromosome breakage or missegregation that can result in micronucleus formation. Detection of micronuclei is a simple, inexpensive, and relatively minimally invasive technique commonly used to evaluate chemical genotoxicity but rarely applied to assess wildlife genotoxic effects. We evaluated the suitability of the micronucleus test as a biomarker of genotoxicity for biomonitoring field studies in bats. We collected blood samples from insectivorous bats roosting in caves surrounded by different levels of disturbance (agriculture, human settlements) in Colima and Jalisco, west central Mexico. Then, we examined the frequency of micronucleus inclusions in erythrocytes using differentially stained blood smears. Bats from caves surrounded by proportionately more (53%) land used for agriculture and irrigated year‐round had higher micronucleus frequency than bats from a less disturbed site (15% agriculture). We conclude that the micronucleus test is a sensitive method to evaluate genotoxic effects in free‐ranging bats and could provide a useful biomarker for evaluating risk of exposure in wild populations. Environ Toxicol Chem 2021;40:202–207.
    [Sandoval‐Herrera, N., Castillo, J.P., Montalvo, L.G.H. and Welch, K.C., 2020. Environmental Toxicology and Chemistry.]