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Mammals

Impacts of Pesticides on Mammals

Mammals can be directly exposed to pesticides, but are most commonly affected indirectly, through groundwater contamination and runoff, or through secondary poisonings such as ingesting prey that has been exposed to pesticides.

  • In 2014, a mountain lion in California was found to be experiencing mange (parasitic mites) as a result of pesticide poisoning due to rodenticides moving up the food chain.
  • In 2012, the U.S. Fish and Wildlife Service (FWS) announced a proposal to list the fisher (part of the weasel family) as threatened under the Endangered Species Act (ESA) due to the impact of rodenticides used in illegal marijuana operations. 
  • Neurotoxicology and Teratology published a study on the neurobehavioral toxicology of pyrethroid insecticides in 2008. Researchers found that decreased motor skills and coordination, slow response rates, and startle responses to noise are other possible effects of pesticide exposure in mammals.
  • Atlantic Bottlenose Dolphins
    Atlantic Bottlenose Dolphins. Photo by Pete Markham
    Research summarizing toxicological data on the effects of the organochlorine pesticides DDT, and its metabolites, found that these organochlorine compounds can impair female fertility by altering ovarian development and function in mammals.
  • Banned in 1972 for its toxic and deadly effects, DDT still persists in the environment and impacts wildlife. Levels of DDT remain dangerously high in some species of marine mammals, such as the short beaked common dolphin, killer whale, and common bottlenose dolphin
  • Evidence, published in Human and Ecological Risk Assessment, has shown that aquatic mammals exposed to general levels of DDT and other, newer pesticides, have impacted reproductive, immune and endocrine function.

[See More Scientific Studies Below]

Economic Cost

Mammals provide many ecosystem services. Some mammals provide food, clothing, and other materials that are used by humans. They provide the opportunity for recreational activities, such as zoos, horseback riding, hunting or animal watching. Other mammals, such as the cow, are revered and worshiped in certain communities for their religious affiliation. All mammals are responsible for ecologic biodiversity in some way, whether it be large or small. For example: bears eat berries and then travel, excreting the berries farther away, which gives plants the ability to spread and grow where they otherwise could not.

Pesticides can and do negatively impact mammals and the ecosystem services they provide, but the full economic impact can be difficult to define. The services listed above may not have a direct price associated with them, but it can be assumed that the impacts of pesticides on mammals cause some economic burden due to loss of ecosystem services. One can assume that prices will climb as mammal populations decline while the demand for the services they provide remains constant. If domesticated mammals that humans depend on for food decline due to pesticide exposure, society would experience an increase in the price of food. Similarly, if there is a drop in the number of mammals that provide biological diversity, ecological stability could easily be threatened, which in turn would affect human life.

Litigation & Lawsuits

Indiana bat
Indiana bat. Photo by USFWSmidwest. 

In 2015, EPA was sued for violating the Endangered Species Act (ESA). The lawsuit documents EPA’s failure to consult with the U.S. Fish and Wildlife Service (FWS) regarding the impact of the herbicide on two endangered species: the Indiana bat (and the whooping crane). A motion was filed against EPA after the decision was made to expand the use of Enlist Duo to nine additional states.

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Scientific Studies: 

  • Associations between fecal chemical pollutants and hormones in primates inhabiting Kibale National Park, Uganda
    While anthropogenic pollutants are known to be a threat to primates, our understanding of exposure to pollutants in situ and their sub-lethal effects is still limited. We used non-invasive biomonitoring to examine associations between faecal concentrations of 97 chemical pollutants and faecal hormone metabolites of cortisol and oestradiol in four primate species inhabiting Kibale National Park, Uganda (chimpanzees—Pan troglodytes, olive baboons—Papio anubis, red colobus—Piliocolobus tephrosceles and red-tailed monkeys—Cercopithecus ascanius). Across all species (n = 71 samples), results demonstrated positive associations of organochlorine pesticides (OCPs) (β = 0.143, p = 0.020) and organophosphate esters (β = 0.112, p = 0.003) with cortisol in adult females. Additionally, we observed positive associations of OCPs (β = 0.192, p = 0.013) and brominated flame retardants (β = 0.176, p = 0.004) with cortisol in juveniles. Results suggest that cumulative pesticides and flame retardants are disruptive to endocrine function in these populations, which could have implications for development, metabolism and reproduction. Our study further demonstrates that faeces can be an important, non-invasive matrix for examining pollutant–hormone associations in wild primates and other critical wildlife populations.
    [Steiniche, T., Wang, S., Chester, E., Mutegeki, R., Rothman, J.M., Wrangham, R.W., Chapman, C.A., Venier, M. and Wasserman, M.D., 2023. Biology Letters, 19(5), p.20230005.]
  • Cetaceans as bio-indicators revealed the increased risks of triclosan exposure and associated thyroid hormone disruption during the COVID-19 pandemic.
    The global surge in disinfection practices from the COVID-19 response has raised concerns about the marine exposure to the hazardous ingredients in disinfectant products, including triclosan (TCS) and triclocarban (TCC). However, there are very limited studies on the response of marine TCS and TCC (TCs) loading to the COVID-19 pandemic. Here we used cetaceans as bio-indicators for a long-term retrospective analysis of TCs loading to the South China Sea (SCS) between 2004 and 2022. Hepatic TCs was 100% detected in all nine cetacean species (n = 120). Interestingly, TCS concentrations decreased in Indo-Pacific humpback dolphins (IPHD) before the pandemic from 2010 to 2017. However, after 2019, TCS concentrations in IPHD significantly increased several-fold. Similarly, post-pandemic TCS concentrations in Indo-Pacific finless porpoises (IPFP) and two fish species were significantly higher than pre-pandemic levels. There were significant relationships between thyroid hormones (THs) and TCs in IPHD and IPFP, suggesting that increased TCs may worsen the interference of THs homeostasis and nutritional conditions in cetaceans. These findings demonstrate the profound impact of the surging use of TCs-containing products from the COVID-19 response on marine ecosystems.
    [Guo, Y., Shi, W., Liu, Z., Sun, X. and Wu, Y., 2023. Journal of Hazardous Materials, 459, p.132289.]
  • Olfactory misinformation reduces wheat seed loss caused by rodent pests
    Alternatives to pesticides are urgently needed to meet sustainable agriculture goals but few options are available for many systems. Here we test how a form of olfactory misinformation on a newly sown wheat crop can prevent wild house mice (Mus musculus) from finding buried seeds. Our misinformation tactic, odour camouflage, reduced seed loss by >63%, providing a simple, non-lethal and ethical way to reduce seed damage and avoid rodenticide use.
    [Parker, F.C., Price, C.J., Bytheway, J.P. and Banks, P.B., 2023. Nature Sustainability, pp.1-4.]
  • The dynamics of persistent organic pollutant (POP) transfer from female bottlenose dolphins (Tursiops truncatus) to their calves during lactation.
    Persistent organic pollutants (POPs) are lipophilic compounds that can accumulate in high concentrations in the blubber of marine mammals, which are long-lived, top-level predators in their ecosystems. These compounds, which include DDTs, PCBs, PBDEs, HCHs, and CHLDs, impact mammalian health, including neurological effects, reduced immune system efficiency, and reproductive failure. POPs are transferred from females to their offspring during gestation and lactation, which have implications for the health of newborn marine mammals, particularly first-born offspring who receive higher concentrations. The dynamics of POP transfer during lactation have been studied in a few pinniped species, but there are no comparable studies on living cetaceans. Because life history strategies and behavior of lactating phocids differ from dolphins, a study on delphinid maternal transfer is warranted. To accomplish this, placenta and longitudinally collected blood and milk samples were taken concurrently from trained bottlenose dolphin, Tursiops truncatus, mother/calf pairs to assess the dynamics of maternal contaminant transfer. Initial POP levels in placenta, blood serum, and milk varied by individual and were related to the age and reproductive history of the females. Regardless of initial POP levels, maternal serum and milk concentrations decreased while calf serum POP levels increased over time. Pollutant transfer varied by POP class and by congener. Contaminant transfer efficiency to calves was most apparent for 4- to 6‑chlorine PCBs, DDT isomers p,p'-DDD, p,p'-DDT, o,p'-DDD, and o,p'-DDE, trans-nonachlor, cis-nonachlor, heptachlor epoxide, nonachlor III, and oxychlordane. By the end of the lactation period, calf serum POP levels were considerably greater than those of their mothers, particularly for compounds with fewer chlorines. POP levels were most biomagnified in the calf born to the primiparous female. These results provide critical information on one component of contaminant transfer in the marine ecosystem and for understanding potential risks of POP exposure to developing odontocete calves.
    [Noren, D.P., Johnson, S., Boyd, D., Ylitalo, G.M., Lundin, J., McCormley, M. and Jensen, E.D., 2023. Science of The Total Environment, p.167888.]
  • Ecosystem Services and Land Rental Markets: Producer Costs of Bat Population Crashes
    Non-market natural capital provides crucial inputs across the economy. In this paper, researchers use land rental market data to calculate the welfare impacts of a change in an unpriced natural capital using well-identified causal impact estimates while accounting for spatial spillovers. The researcher apply the welfare analysis to examine the cost of whitenose syndrome (WNS) in bats, which provide pest control services to agricultural producers. WNS, a disease that decimates infected bat populations, began spreading through the US starting in the mid-2000s. We find that the loss of bats in a county causes land rental rates.
    [Manning, D. and Ando, A.]
  • The chemical landscape of tropical mammals in the Anthropocene
    Sixty years ago, Rachel Carson published her book Silent Spring, which focused the world's attention on the dangers of pesticides. Since that time human impacts on the environment have accelerated and this has included reshaping the chemical landscape. Here we evaluate the severity of exposure of tropical terrestrial mammals to pesticides, pharmaceuticals, plastics, particulate matter associated with forest fires, and nanoparticles. We consider how these environmental contaminants interact with one another, with the endocrine and microbiome systems of mammals, and with other environmental changes to produce a larger negative impact than might initially be expected. Using this background and building on past conservation success, such as mending the ozone layer and decreasing acid rain, we tackle the difficult issue of how to construct meaningful policies and conservation plans that include a consideration of the chemical landscape. We document that policy solutions to improving the chemical landscape are already known and the path of how to construct a healthier planet is discernible.
    [Chapman, C.A., Steiniche, T., Benavidez, K.M., Sarkar, D., Amato, K., Serio-Silva, J.C., Venier, M. and Wasserman, M.D., Biological Conservation, 269, p.109522.]
  • Agricultural Fast Food: Bats Feeding in Banana Monocultures Are Heavier but Have Less Diverse Gut Microbiota
    Habitat alteration for agriculture can negatively affect wildlife physiology and health by decreasing diet diversity and increasing exposure to agrochemicals for animals foraging in altered landscapes. Such negative effects may be mediated by the disruption of the gut microbiota (termed dysbiosis), yet evidence for associations between habitat alteration, wildlife health, and the gut microbiota remains scarce. We examine the association between management intensity of banana plantations and both the body condition and gut microbiota composition of nectar-feeding bats Glossophaga soricina, which commonly forage within banana plantations across Latin America. We captured and measured 196 bats across conventional monocultures, organic plantations, and natural forests in Costa Rica, and quantified gut microbiome bacterial phylogenetic diversity using 16S rRNA amplicon sequencing. We found that gut microbiota from bats foraging in conventional monocultures were overall less phylogenetically diverse than those from bats foraging in organic plantations or natural forests, both of which were characterized by diverse bacterial assemblages and individualized microbiota. Despite lower diversity, co-occurrence network complexity was higher in conventional monocultures, potentially indicating altered microbial interactions in agricultural landscapes. Bats from both organic and conventional plantations tended to be larger and heavier than their forest counterparts, reflecting the higher food supply. Overall, our study reveals that whilst both conventional monocultures and organic plantations provide a reliable food source for bats, conventional monocultures are associated with less diverse and potentially dysbiotic microbiota, whilst organic plantations promote diverse and individualized gut microbiota akin to their natural forest-foraging counterparts. Whilst the long-term negative effects of anthropogenically-altered microbiota are unclear, our study provides further evidence from a novel perspective that organic agricultural practices are beneficial for wildlife health.
    [Alpízar, P., Risely, A., Tschapka, M. and Sommer, S. Frontiers in Ecology and Evolution, p.608.]
  • Anthropogenic Contaminants and Histopathological Findings in Stranded Cetaceans in the Southeastern United States, 2012–2018
    Anthropogenic contaminants in the marine environment often biodegrade slowly, bioaccumulate in organisms, and can have deleterious effects on wildlife immunity, health, reproduction, and development. In this study, we evaluated tissue toxicant concentrations and pathology data from 83 odontocetes that stranded in the southeastern United States during 2012–2018. Mass spectrometry was used to analyze blubber samples for five organic toxicants (atrazine, bisphenol-A, diethyl phthalates, nonylphenol monoethoxylate [NPE], triclosan), and liver samples were analyzed for five non-essential elements (arsenic, cadmium, lead, mercury, thallium), six essential elements (cobalt, copper, manganese, iron, selenium, zinc) and one toxicant mixture class (Aroclor1268). Resultant data considerably improve upon the existing knowledge base regarding toxicant concentrations in stranded odontocetes. Toxicant and element concentrations varied based on animal demographic factors including species, sex, age, and location. Samples from bottlenose dolphins had significantly higher average concentrations of lead, manganese, mercury, selenium, thallium, and zinc, and lower average concentrations of NPE, arsenic, cadmium, cobalt, and iron than samples from pygmy sperm whales. In adult female bottlenose dolphins, average arsenic concentrations were significantly higher and iron concentrations were significantly lower than in adult males. Adult bottlenose dolphins had significantly higher average concentrations of lead, mercury, and selenium, and significantly lower average manganese concentrations compared to juveniles. Dolphins that stranded in Florida had significantly higher average concentrations of lead, mercury, and selenium, and lower concentrations of iron than dolphins that stranded in North Carolina. Histopathological data are presented for 72 animals, including microscopic evidence of Campula spp. and Sarcocystis spp. infections, and results of Morbillivirus and Brucella spp. molecular diagnostic testing. Sublethal cellular changes related to toxicant exposure in free-ranging odontocetes may lead to health declines and, in combination with other factors, may contribute to stranding.
    [Page-Karjian, A., Lo, C.F., Ritchie, B., Harms, C.A., Rotstein, D.S., Han, S., Hassan, S.M., Lehner, A.F., Buchweitz, J.P., Thayer, V.G. and Sullivan, J.M., 2020. Frontiers in Marine Science, 7, p.630.]
  • Long-term maternal exposure to atrazine in the drinking water reduces penis length in the tammar wallaby Macropus eugenii
    Marsupials are experiencing devastating population declines across Australia. Exposure to environmental endocrine disruptors, through ingestion of contaminated resources in the environment, could be contributing to this decline. Atrazine (ATZ), a widely used herbicide in Australia, is an endocrine disruptor with the ability to cause reproductive abnormalities in a diverse range of vertebrates. We exposed adult female wallabies (Macropus eugenii) to drinking water containing ATZ (450 p.p.m) throughout pregnancy, parturition and lactation. We assessed the outcome of this exposure to the reproductive development of their young by assessing gonad and phallus development. Both these organs are especially sensitive to perturbations in the hormonal environment during development. Although no gross abnormalities were seen in gonad structure, exposure to ATZ did alter the expression of genes required for normal testis function. Furthermore, long-term exposure to ATZ resulted in a significant reduction in penis length. These results demonstrate that ATZ exposure during gestation and lactation can significantly affect the development of male young by affecting virilisation. Given the known vulnerability of macropodid marsupials to endocrine disruption, as well as their overlapping distribution with agricultural areas, these data raise major concerns for the use of pesticides in areas with fragile marsupial populations.
    [Cook, L.E., Chen, Y., Renfree, M.B. and Pask, A.J., 2020. Reproduction, Fertility and Development, 32(13), pp.1168-1168.]
  • 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.]
  • Partitioning of persistent organic pollutants between blubber and blood of wild bottlenose dolphins: implications for biomonitoring and health
    Biomonitoring surveys of wild cetaceans commonly utilize blubber as a means to assess exposure to persistent organic pollutants (POPs), but the relationship between concentrations in blubber and those in blood, a better indicator of target organ exposure, is poorly understood. To define this relationship, matched blubber and plasma samples (n = 56) were collected from free-ranging bottlenose dolphins (Tursiops truncatus) and analyzed for 61 polychlorinated biphenyl (PCB) congeners, 5 polybrominated diphenyl ether (PBDE) congeners, and 13 organochlorine pesticides (OCPs). With the exception of PCB 209, lipid-normalized concentrations of the major POPs in blubber and plasma were positively and significantly correlated (R(2) = 0.828 to 0.976). Plasma concentrations, however, significantly increased with declining blubber lipid content, suggesting that as lipid is utilized, POPs are mobilized into blood. Compound- and homologue- specific blubber/blood partition coefficients also differed according to lipid content, suggesting POPs are selectively mobilized from blubber. Overall, these results suggest that with the regression parameters derived here, blubber may be used to estimate blood concentrations and vice versa. Additionally, the mobilization of lipid from blubber and concomitant increase in contaminants in blood suggests cetaceans with reduced blubber lipid may be at greater risk for contaminant-associated health effects.
    [Yordy JE, Wells RS, Balmer BC, Schwacke LH, Rowles TK, Kucklick JR. 2010. Environ Sci Technol. 15;44(12):4789-95]
  • Mammary Gland Development as a Sensitive End Point after Acute Prenatal Exposure to an Atrazine Metabolite Mixture in Female Long-Evans Rats
    Atrazine (ATR), a widely used chlorotriazine herbicide, inhibits a number of endocrine-dependent processes, including gonadotrophin surges and mammary gland development in rats. Chlorotriazine herbicides are rapidly metabolized in plants and animals to form a group of metabolites that are detected both in the environment and in exposed animals. The extent to which these metabolites are responsible directly for the observed health effects is not understood. Our goal was to determine if a mixture of ATR metabolites, in proportions found in the environment, might produce developmental effects in Long-Evans rats following exposure late in pregnancy. We administered an ATR metabolite mixture (AMM) containing ATR, hydroxyatrazine, diaminochlorotriazine, deethylatrazine, and deisopropylatrazine orally to pregnant Long-Evans rats at 0.09, 0.87, or 8.73 mg/kg body weight (bw)/day, on gestation days 15–19, using 0 and 100 mg ATR/kg bw/day as negative and positive controls, respectively. We observed no significant effect of acute AMM exposure on body weight gain in dams during the dosing period, weight loss in pups on postnatal day (PND)4, or pubertal timing, as is seen with ATR alone. However, as with ATR, we detected delayed mammary gland development, evaluated by whole mount analysis, as early as PND4 in all treatment groups. Our data suggest that acute exposure to AMM at levels as low as 0.09 mg/kg bw during late pregnancy causes persistent alterations in mammary gland development of female offspring, and that these effects do not appear to be related to bw or associated with pubertal timing.
    [Enoch R.R., et al. 2007. Environmental Health Perspectives, 115(4).]