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The chemical landscape of tropical mammals in the Anthropocene

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Abstract

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.

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Deltamethrin (DTM) is a pyrethroid insecticide widely used for agricultural purposes. Exposure to DTM has proven to be harmful to humans, but whether low, environmental concentrations of this pesticide also poses a threat to wild mammals is still unknown. In Neotropical areas, bats play important roles in contributing to forest regeneration. We investigated the effects of DTM exposure on the reproductive function of male Neotropical fruit-eating bats (Artibeus lituratus), known for contributing to reforestation through seed dispersal in Neotropical Forests. Bats were assigned to 3 groups: control (fed with papaya); DTM2 (fed with papaya treated with DTM at 0.02 mg/kg) and DTM4 (fed with papaya treated with DTM at 0.04 mg/kg) for seven days. Bats from DTM2 and DTM4 groups showed increased testicular levels of nitric oxide and superoxide dismutase and catalase activities. The germinal epithelium from DTM4 bats showed non-viable cells and cell desquamation, indicating microscopic lesions and Leydig cells atrophy. Our results demonstrate the onset of cell degeneration that may affect the reproductive function in DTM exposed bats.
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Bwindi Impenetrable National Park situated southwest of Uganda is a biodiversity hotspot that is home to about half of the world's endangered mountain gorilla (Gorilla beringei). Given its ecological significance and mounting pressures from agricultural activities such as tea growing, continuous monitoring of the levels of chemical toxins like pesticides in the park and surrounding areas is needed for effective conservation strategies. Furthermore, persistent organochlorine pesticides (OCPs) like DDT were used in agricultural gardens and indoor spraying in Kanungu district between the 1950s and 80s. The focus of this study was to explore the possible exposure of mountain gorillas to OCPs and cypermethrin used by the farmers in the areas near the park. Data from our interviews revealed that glyphosate is the most widely used pesticide by the farmers in areas surrounding the park, followed by cypermethrin, and mancozeb. Samples of leaves from plants consumed by mountain gorillas along the forest edges of the park and surficial soils (15–20 cm depths) were collected from three sites (Ruhija, Nkuringo and Buhoma) and analysed for the presence of cypermethrin and OCPs residues. Concentrations of total (∑) DDTs and ∑endosulfans were up to 0.34 and 9.89 mg/kg dry weight (d.w), respectively in soil samples. Concentrations of ∑DDTs and ∑endosulfans in samples of leaves ranged from 0.67 to 1.38 mg/kg d.w (mean = 1.07 mg/kg d.w) and 0.9 to 2.71 mg/kg d.w (mean = 1.68 mg/kg d.w), respectively. Mean concentration of ∑DDTs in leaves exceeded the European pharmacopeia and United States pharmacopeia recommended maximum residue limit values for DDTs in medicinal plants (1.0 mg/kg). In addition, calculated hazard indices for silverbacks (36.35), females (57.54) and juveniles (77.04) suggested potential health risks to the mountain gorillas. o,p′-DDT/p,p′-DDT ratios (0.5–0.63) in samples of leaves confirmed recent input of dicofol-DDT type in Bwindi rainforest.
Article
ContextThe Cerrado is a Global Biodiversity Hotspot as well as Brazil’s main frontier for large-scale agriculture and livestock production, making it one of the most threatened biomes in the country. Brazil is one of the biggest consumers of pesticides in the world and allows the use of chemicals that are banned in many other countries due to their adverse health effects in a wide range of species, including humans. AimsThis study aimed to assess pesticide and metal exposure of the lowland tapir – a threatened, large herbivorous mammal – to support future studies of the role of these chemicals in tapir health, survivorship, and population viability. Methods Foot pad, proboscis, stomach contents, liver, bone, and nail samples were obtained from tapir carcasses found along highways (n=87). (i) Atomic absorption spectrophotometry (AAS) was used to detect metals in bone, nail and liver tissue; (ii) gas chromatography – nitrogen phosphorous detector (GC-NPD) to detect organophosphates in liver and skin; and (iii) high performance liquid chromatography – ultraviolet (HPLC-UV) to detect pyrethroids and carbamates in stomach contents. Key resultsTwo carbamates (aldicarb and carbaryl), three organophosphates (diazinon, malathion, and mevinphos), two pyrethroids (deltamethrin and permethrin), and two toxic metals (cadmium and lead) were detected in different tapir tissue samples, some at concentrations high enough to cause adverse health effects. In 90% of roadkill tapirs that were subjected to a full post-mortem examination (n=25), macroscopic alterations of liver and/or kidney tissue were observed. Conclusions This study provides the first report to date of the detection of pesticides and metals in lowland tapirs. ImplicationsSome of the reported pesticide concentrations exceed environmental safety thresholds. Consequently, results from this study raise concerns over potential adverse health effects in tapirs that could lead to population level impacts, thus requiring further investigation.
Article
Bats provide a variety of ecological services that are essential to the integrity of ecosystems. Indiscriminate use of pesticides has been a threat to biodiversity, and the exposure of bats to these xenobiotics is a threat to their populations. This study presents a review of articles regarding the exposure of bats to pesticides published in the period from January 1951 to July 2020, addressing the temporal and geographical distribution of research, the studied species, and the most studied classes of pesticides. The research was concentrated in the 1970s and 1980s, mostly in the Northern Hemisphere, mainly in the USA. Of the total species in the world, only 5% of them have been studied, evaluating predominantly insectivorous species of the Family Vespertilionidae. Insecticides, mainly organochlorines, were the most studied pesticides. Most research was observational, with little information available on the effects of pesticides on natural bat populations. Despite the advances in analytical techniques for detecting contaminants, the number of studies is still insufficient compared to the number of active ingredients used. The effects of pesticides on other guilds and tropical species remain poorly studied. Future research should investigate the effects of pesticides, especially in sublethal doses causing chronic exposure. It is crucial to assess the impact of these substances on other food guilds and investigate how natural populations respond to the exposure to mixtures of pesticides found in the environment.
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Although the behaviour and ecology of primates have been more thoroughly studied than that of any other group of mammals, there have been very few attempts to compare the communities of living primates found in different parts of the world. In Primate Communities, an international group of experts compares the composition, behaviour and ecology of primate communities in Africa, Asia, Madagascar and South America. They examine the factors underlying the similarities and differences between these communities, including their phylogenetic history, climate, rainfall, soil type, forest composition, competition with other vertebrates and human activities. As it brings together information about primate communities from around the world for the very first time, it will quickly become an important source book for researchers in anthropology, ecology and conservation, and a readable and informative text for undergraduate and graduate students studying primate ecology, primate conservation or primate behaviour.
Article
The habitats of wild primates are increasingly threatened by surrounding anthropogenic pressures, but little is known about primate exposure to frequently used chemicals. We applied a novel method to simultaneously measure 21 legacy pesticides (OCPs), 29 current use pesticides (CUPs), 47 halogenated flame retardants (HFRs), and 19 organophosphate flame retardants in feces from baboons in the U.S.A., howler monkeys in Costa Rica, and baboons, chimpanzees, red-tailed monkeys, and red colobus in Uganda. The most abundant chemicals were α-hexachlorocyclohexane (α-HCH), β-hexachlorocyclohexane (β-HCH), and hexachlorobenzene among OCPs across all sites, chlorpyrifos among CUPs in Costa Rica and Indiana, decabromodiphenylethane (DBDPE) in Costa Rica and Indiana and 2, 2', 4, 4'-tetrabromodiphenyl ether (BDE-47) in Uganda as HFRs, and tris(2-butoxyethyl) phosphate (TBOEP) as OPFRs across all sites. The detected chemical concentrations were generally higher in red-tailed monkeys and red colobus than in chimpanzees and baboons. Our methods can be used to examine the threat of chemical pollutants to wildlife, which is critical for endangered species where only noninvasive methods can be used.
Article
Here, there, and everywhere No place is safe from plastic pollution. Brahney et al. show that even the most isolated areas in the United States—national parks and national wilderness areas—accumulate microplastic particles after they are transported there by wind and rain (see the Perspective by Rochman and Hoellein). They estimate that more than 1000 metric tons per year fall within south and central western U.S. protected areas. Most of these plastic particles are synthetic microfibers used for making clothing. These findings should underline the importance of reducing pollution from such materials. Science , this issue p. 1257 ; see also p. 1184
Article
The gut is a first point of contact with ingested xenobiotics, where chemicals are metabolized directly by the host or microbiota. Atrazine is a widely used pesticide, but the role of the microbiome metabolism of this xenobiotic and the impact on host responses is unclear. We exposed successive generations of the wasp Nasonia vitripennis to subtoxic levels of atrazine and observed changes in the structure and function of the gut microbiome that conveyed atrazine resistance. This microbiome-mediated resistance was maternally inherited and increased over successive generations, while also heightening the rate of host genome selection. The rare gut bacteria Serratia marcescens and Pseudomonas protegens contributed to atrazine metabolism. Both of these bacteria contain genes that are linked to atrazine degradation and were sufficient to confer resistance in experimental wasp populations. Thus, pesticide exposure causes functional, inherited changes in the microbiome that should be considered when assessing xenobiotic exposure and as potential countermeasures to toxicity.
Article
This study aimed to assess the distribution of spent pesticides in an agro-farming area and to evaluate their impact on the ecological risk for an endangered species combing the health risk assessment concept with the modelling algorithm proposed by European Food Safety Authority (EFSA). An agricultural area in western Taiwan was chosen to investigate the ecological risk on Prionailurus bengalensis. Their ecological stability was evaluated in the context of the residuals' distribution of the spent pesticides in the investigated area. The pesticide residues accumulated and correlated highly to the adverse health impact on the leopard cat. In the present study, 67 pesticides were detected from 79 collected soil samples. The hazard index (HI) was found related to land use patterns and the HI values in Yuanli and Zhuolan were significantly higher than those in the other areas, increasing poisoning probability of the leopard cat. The locations of agro-chemical utilization were highly overlapped with leopard cats' activity zone, supporting the hypothesis that pesticide residues posed a potential threat to the leopard cats' health. The proposed risk assessment framework was capable of estimating the risk caused by pesticide residues and no similar study has been reported before.
Article
Microplastics are ubiquitous environmental contaminants leading to inevitable human exposure. Even so, little is known about the effects of microplastics in human health. Thus, in this work we review the evidence for potential negative effects of microplastics in the human body, focusing on pathways of exposure and toxicity. Exposure may occur by ingestion, inhalation and dermal contact due to the presence of microplastics in products, foodstuff and air. In all biological systems, microplastic exposure may cause particle toxicity, with oxidative stress, inflammatory lesions and increased uptake or translocation. The inability of the immune system to remove synthetic particles may lead to chronic inflammation and increase risk of neoplasia. Furthermore, microplastics may release their constituents, adsorbed contaminants and pathogenic organisms. Nonetheless, knowledge on microplastic toxicity is still limited and largely influenced by exposure concentration, particle properties, adsorbed contaminants, tissues involved and individual susceptibility, requiring further research.
Article
Over 40 years of regulations in the United States have failed to protect human and environmental health. We contend that these failures result from the flawed governance over the continued production, use, and disposal of toxic chemicals. To address this failure, we need to identify the broader social, political, and technological processes producing, knowing, and regulating toxic chemicals, collectively referred to as toxic chemical governance. To do so, we create a conceptual framework covering five key domains of governance: knowledge production, policy design, monitoring and enforcement, evaluation, and adjudication. Within each domain, social actors of varying power negotiate what constitutes acceptable risk, creating longer-term path dependencies in how they are addressed (or not). Using existing literature and five case studies, we discuss four paths for improving governance: evolving paradigms of harm, addressing bias in the knowledge base, making governance more equitable, and overcoming path dependency.
Article
Microplastics are ubiquitous across ecosystems, yet the exposure risk to humans is unresolved. Focusing on the American diet, we evaluated the number of microplastic particles in commonly consumed foods in relation to their recommended daily intake. The potential for microplastic inhalation and how the source of drinking water may affect microplastic consumption were also explored. Our analysis used 402 data points from 26 studies, which represents over 3600 processed samples. Evaluating approximately 15% of Americans' caloric intake, we estimate that annual microplastics consumption ranges from 39000 to 52000 particles depending on age and sex. These estimates increase to 74000 and 121000 when inhalation is considered. Additionally, individuals who meet their recommended water intake through only bottled sources may be ingesting an additional 90000 microplastics annually, compared to 4000 microplastics for those who consume only tap water. These estimates are subject to large amounts of variation; however, given methodological and data limitations, these values are likely underestimates.
Article
Protected areas have developed alongside intensive changes in land use and human settlements in the neighboring landscape. Here, we investigated the occurrence of 21 organochlorine pesticides (OCPs), 14 current use pesticides (CUPs), 47 halogenated flame retardants (HFRs), and 19 organophosphate esters (OPEs) in air around Las Cruces (LC) and La Selva (LS) Biological Stations, Costa Rica, and Kibale National Park (KNP), Uganda using passive air samplers (PAS) with polyurethane foam (PUF) discs (PAS-PUF). Significantly higher concentrations of CUPs were observed around LS, while LC had a higher concentration of OCPs. Land use analysis indicated that LS had a higher fraction of agriculture than LC (33% vs 14%), suggesting the higher CUPs concentration at LS was related to pesticide intensive crops, while higher OCPs concentration at LC may be attributed to the area's long agricultural history characterized by small-scale subsistence farming or long-range transport. In Uganda, CUPs and OCPs were generally lower than in Costa Rica, but high concentrations of HFRs were observed inside KNP, possibly due to human activity at research camps near the protected forest. This is the first study that documented the occurrence of anthropogenic chemicals in the air at protected areas with tropical forests.
Article
As small pieces of plastics known as microplastics pollute even the remotest parts of Earth, research currently focuses on unveiling how this pollution may affect biota. Despite increasing awareness, one potentially major consequence of chronic exposure to microplastics has been largely neglected: the impact of the disruption of the symbiosis between host and the natural community and abundance pattern of the gut microbiota. This so-called dysbiosis might be caused by the consumption of microplastics, associated mechanical disruption within the gastrointestinal tract, the ingestion of foreign and potentially pathogenic bacteria, as well as chemicals, which make-up or adhere to microplastics. Dysbiosis may interfere with the host immune system and trigger the onset of (chronic) diseases, promote pathogenic infections, and alter the gene capacity and expression of gut microbiota. We summarize how chronically exposed species may suffer from microplastics-induced gut dysbiosis, deteriorating host health, and highlight corresponding future directions of research.
Article
Pesticide pollution residues have become increasingly common health hazards over the last several decades because of the wide use of pesticides. The gastrointestinal tract is the first physical and biological barrier to contaminated food and is therefore the first exposure site. Interestingly, a number of studies have shown that the gut microbiota plays a key role in the toxicity of pesticides and has a profound relationship with environmental animal and human health. For instance, intake of the pesticide of chlorpyrifos can promote obesity and insulin resistance through influencing gut and gut microbiota of mice. In this review, we discussed the possible effects of different kinds of widely used pesticides on the gut microbiota in different experimental models and analyzed their possible subsequent effects on the health of the host. More and more studies indicated that the gut microbiota of animals played a very important role in pesticides-induced toxicity, suggesting that gut micriobita was also the unintended recipient of pesticides. We hope that more attention can focus on the relationship between pesticides, gut microbiota and environmental health risk assessment in near future.
Article
Hormonal growth promoters (HGPs), widely used in beef cattle production globally, make their way into the environment as agricultural effluent—with potential impacts on aquatic ecosystems. One HPG of particular concern is 17β-trenbolone, which is persistent in freshwater habitats and can affect the development, morphology and reproductive behaviors of aquatic organisms. Despite this, few studies have investigated impacts of 17β-trenbolone on non-reproductive behaviors linked to growth and survival, like boldness and predator avoidance. None consider the interaction between 17β-trenbolone and other environmental stressors, such as temperature, although environmental challenges confronting animals in the wild seldom, if ever, occur in isolation. Accordingly, this study aimed to test the interactive effects of trenbolone and temperature on organismal behavior. To do this, eastern mosquitofish (Gambusia holbrooki) were subjected to an environmentally-relevant concentration of 17β-trenbolone (≤5.1 ± 0.5 ng/L) or freshwater (i.e. control) for 21 days under one of two temperatures (20 and 30 °C), after which the predator escape, boldness and exploration behavior of fish were tested. Predator escape behavior was assayed by subjecting fish to a simulated predator strike, while boldness and exploration were assessed in a separate maze experiment. We found that trenbolone exposure increased boldness behavior. Interestingly, some behavioral effects of trenbolone depended on temperature, sex, or both. Specifically, significant effects of trenbolone on male predator escape behavior were only noted at 30 °C, with males becoming less reactive to the simulated threat. Further, in the maze experiment, trenbolone-exposed fish explored the maze faster than control fish, but only at 20 °C. We conclude that field detected concentrations of 17β-trenbolone can impact ecologically important behaviors of fish, and such effects can be temperature dependent. Such findings underscore the importance of considering the potentially interactive effects of other environmental stressors when investigating behavioral effects of environmental contaminants.
Chapter
Most primate habitats are undergoing intense and rapid changes due to anthropogenic influences resulting in many primate populations being threatened. Habitat loss and fragmentation are already extensive; thus dispersal to unoccupied habitats is an unlikely adaptive response to these changes. Furthermore, most primates have slow life histories and long generation times, and because environmental change is occurring at an unprecedented rate, gene-based adaptations are also unlikely to evolve fast enough to offer successful responses to these changes. However, long primate life histories are linked to well-developed brains, which may allow primates to respond to environmental change through behavioural flexibility. Here we ask: What are the most common challenges of changing environments for primates and what do we know about their behavioural abilities to respond to such changes? To answer this question, we first review the most common types of habitat/landscape alterations, the extent of human-primate interactions, and the impact of climate change. Next, we evaluate how primates respond to these changes via behavioural flexibility, and using different approaches and datasets, we discuss how to investigate if these responses are beneficial with regard to population persistence. Finally, we discuss how comparisons across species, space, and time can be used to draw generalizations about primate responses to environmental change while considering their behavioural flexibility and the data derived from case studies. We demonstrate how understanding behavioural flexibility as a response to environmental change will be crucial to optimize conservation efforts by constructing informed management plans.
Article
Probiotics are widely prescribed for prevention of antibiotics-associated dysbiosis and related adverse effects. However, probiotic impact on post-antibiotic reconstitution of the gut mucosal host-microbiome niche remains elusive. We invasively examined the effects of multi-strain probiotics or autologous fecal microbiome transplantation (aFMT) on post-antibiotic reconstitution of the murine and human mucosal microbiome niche. Contrary to homeostasis, antibiotic perturbation enhanced probiotics colonization in the human mucosa but only mildly improved colonization in mice. Compared to spontaneous post-antibiotic recovery, probiotics induced a markedly delayed and persistently incomplete indigenous stool/mucosal microbiome reconstitution and host transcriptome recovery toward homeostatic configuration, while aFMT induced a rapid and near-complete recovery within days of administration. In vitro, Lactobacillus-secreted soluble factors contributed to probiotics-induced microbiome inhibition. Collectively, potential post-antibiotic probiotic benefits may be offset by a compromised gut mucosal recovery, highlighting a need of developing aFMT or personalized probiotic approaches achieving mucosal protection without compromising microbiome recolonization in the antibiotics-perturbed host.
Article
Nanomaterials (NMs) have gained prominence in technological advancements due to their tunable physical, chemical and biological properties wtih enhanced performance over their bulk counterparts. NMs are categorized depending on their size, composition, shape, and origin. The ability to predict the unique properties of NMs increases the value of each classification. Due to increased growth of production of NMs and their industrial applications, issues relating toxicity are inevitable. The aim of this review is to compare the man-made (engineered) and naturally occurring nanoparticles (NPs) and nanostructured materials (NSMs) to identify their nanoscale properties and to define the specific knowledge gaps related to the risk assessment of the NPs and NSMs in the environment. The review presents an overview of NMs history and classifications as well as profiling various sources of NPs and NSMs from natural to synthetic and their toxic effects towards mammalian cells and tissues. Additionally, the types of toxic reactions associated with NPs and NSMs and the regulations implemented by different countries to reduce the risks are also discussed.