Hormesis induced by silver iodide, hydrocarbons, microplastics, pesticides, and pharmaceuticals: Implications for agroforestry ecosystems health
Graphical abstract
Introduction
Forests provide fuelwood and timber to local communities as well as ecosystem services, such as the protection of hydrogeological systems, regulation of water, and maintenance of biodiversity (Binder et al., 2017; Bakker et al., 2019). Thus, they help to alleviate anthropogenic and non-anthropogenic environmental impacts including air pollution, climate change, and hydrogeological risks (Sicard et al., 2018; Santoro et al., 2020). Forests sequester considerable amounts of carbon, thus removing CO2 from the atmosphere, while biomass from wood byproducts, such as bark, black liquor, and wood residues, provide raw materials for the production of renewable energies through gasification and pyrolysis (Wang et al., 2021a).
Forests reduce land surface temperatures (Schwaab et al., 2021) and remove a considerable amount of carbon from the atmosphere (Yu et al., 2021). For example, biomass carbon increment in the planted forests of China would range from 1.23 to 2.13 Pg C from 2010 to 2050, depending on the management (Yu et al., 2021). Forests also reduce human stress, provide rich sources of plant and microbial chemicals used for medicines and nutrition, make food available and offer food safety to vulnerable groups of the population, and help to regulate infectious diseases (Karjalainen et al., 2010). Hence, forests play a key role in pursuing and ensuring carbon neutrality (Wang et al., 2021a), however, these ecosystems also facilitate and promote the improvement of human physical and mental health.
A total of 411 Mha of global tree cover has been lost from 2001 to 2020 due to forestry, wildfire, shifting agriculture, urbanization, and commodity-driven deforestations (Data source: https://www.globalforestwatch.org/ -Accessed on 9 January 2022; Curtis et al. (2018)). Increased deforestation is of concern due to reduced air quality and increased temperatures and loss of clean water, calling for better management strategies (Meijaard et al., 2013). More and improved forest-water reuse systems are needed to ensure water availability and quality (McEachran et al., 2018). These are slow-rate irrigation systems infiltrating treated wastewater from agricultural, industrial, and municipal sources into forest soil and groundwater (McEachran et al., 2018). Increasing deposition of silver iodide (AgI) used in weather modification programs and emerging contaminants, including pharmaceuticals, microplastics and pesticides in the agricultural, industrial, and municipal systems (McEachran et al., 2018), can lead to increased concentrations in forests and agroforestry systems. Moreover, natural fires, storms, and rainfalls contribute to spreading emerging contaminants in forests and agroforestry systems, leading to further local contamination (McEachran et al., 2017; Campo et al., 2017). Hence, there is a need for better ecological risk assessments, which predict the effects of emerging contaminants incorporating hormesis.
Hormesis is a biphasic dose response resulting from contrasting effects between low and high doses/concentrations of a chemical or a blend of chemicals (Fig. 1) (Cutler, 2013). Doses smaller than the toxicological threshold (NOAEL: no-observed-adverse-effect-level) lead to enhanced growth, biomass production, and yields of plants (Jalal et al., 2021; Shahid et al., 2020; Erofeeva, 2022) or stimulation of bioluminescence, biofilm formation, growth, and motility of microbes (Calabrese, 2017; Iavicoli et al., 2021; Agathokleous et al., 2022; Tang et al., 2022). They also lead to improved reproduction and prolonged lifespan of animals (Berkel and Cacan, 2021; Lopes et al., 2020). These stimulatory responses to low doses are typically no more than 60% greater than the control response, and represent adaptive responses aiding organisms to protect themselves against more massive stress and increase their survival odds (Jalal et al., 2021; Calabrese et al., 2019; Schirrmacher, 2021). Hormesis is linked with both acclimation and phenotypic plasticity, being fully supported by ecological and evolutionary theory (Costantini, 2019; Costantini and Borremans, 2019). Numerous chemicals including pollutants1 and emerging contaminants were found to induce hormesis, which emerges as a general phenomenon occurring from local to planetary scales (Erofeeva, 2022; Agathokleous et al., 2022; Schirrmacher, 2021; Agathokleous and Calabrese, 2020). The antithesis in the responses/effects between low (sub-NOAEL) doses and high (super-NOAEL) doses, is now a rule rather than exception, suggesting that any estimation of ecological risks that results from procedures not considering hormetic responses can be strikingly incorrect and misleading.
Here, we reviewed the hormesis induced by AgI and major emerging contaminants of forests and agroforestry systems, viz. pharmaceuticals, microplastics, hydrocarbons, and pesticides. These categories of contaminants were selected for inclusion based on timeliness and a preliminary literature survey, which indicated sufficient evidence permitting assessment of hormesis. We aimed at examining whether such chemically diverse contaminants commonly lead to similar hormetic responses in a plethora of living organisms, independently of taxonomic and functional groups. Then, we aimed at drawing general conclusions about responses to low, sub-NOAEL doses across organisms and types of contaminants, also hypothesizing that hormetic responses would start at lower doses in susceptible than in resistant groups of organisms independently of chemicals and life-form. We summarized the current state of the art and consolidate the positive and negative effects induced by doses smaller than the NOAEL level within the framework of hormesis. We showed that such effects have severe consequences for the agendas of combating or controlling antibiotic and other drug resistance, diseases, disease vectors, and pests, among others, yet they are not captured by the current risk assessments. The ultimate goal of this study is to demonstrate generality of contaminant-induced hormesis, indicating the need for incorporating hormesis into the regulatory risk assessment and considering it in policies directed to protect the health of forest and agroforestry ecosystems as well as the wellbeing and welfare of humans living in forested areas settlements.
Section snippets
Silver iodide
AgI is an efficient nucleus for ice crystal formation used since the 1940s for inducing precipitation in cumulus and layer clouds within 20–25 min from cloud seeding, and is used in many countries nowadays to induce both rain and snowfall (Warner and Twomey, 1956; Friedrich et al., 2020). In December 2020, China's state council announced expansion of the weather modification program to cover an area larger than 5.5 million Km2 by 2025.2
Pharmaceuticals
The global chemical industry's production capacity increased from approximately 1.2 to 2.3 billion tons between 2000 and 2017, and environmental pollution with chemicals is growing (UN Environment, 2019). The sector of healthcare exhibits a considerable global material footprint, reaching 3.6 billion tons in 2015 alone (UN Environment, 2019). Around 630 pharmaceuticals and their transformation products are found in the environment worldwide (aus der Beek et al., 2016), which result from animal
Microplastics
Global production of plastics increased from 1.5 million tons to 3505 million tons between 1950 and 2017 (UN Environment, 2019). About 8 Mt. plastics are discarded yearly into the environment worldwide, eventually decomposing into micro and nano plastics (UN Environment, 2019; González-Fernández et al., 2021; Bradney et al., 2019). About 80% of the microplastics contained in municipal sewage may also end up in sludge spread over forests or farms (Talvitie et al., 2017). Hence, micro (≥1 μm < 5
Hydrocarbons
Hydrocarbons are hydrophobic chemicals, unless bearing a carboxyl (acid; COOH) or another ionized functional group, and the more hydrophobic contaminants may be more abundant in soils than in groundwater (McEachran et al., 2017). Hydrocarbon contamination, including polycyclic aromatic hydrocarbons (PAHs) resulting from incomplete combustion of organic matter, is an old environmental issue and widely occurs in different environmental compartments across the planet) (Samanta et al., 2002; Pérez
Pesticides
Around 600 pesticides are in use, while some are classified as highly hazardous (UN Environment, 2019) and deposit into the environment over time. The use of pesticide may increase due to climate change driven increasing pest attacks such as locusts (UN Environment, 2019; Botten et al., 2021; Peng et al., 2020). A number of pesticides are applied to agroforests directly or via the use of treated municipal wastewater. Pesticide residues are also found in forests worldwide (see Supplementary
Sub-NOAEL effects: the general picture
Hormesis commonly occurs in a vast array of living organisms exposed to major agroforestry contaminants, illustrating that positive or negative effects occur at sub-NOAEL doses. Hence, the need to consider such sub-NOAEL effects in both research and risk assessment agendas has emerged. Sub-NOAEL doses of AgI, human and veterinary pharmaceuticals, microplastics, hydrocarbons, and pesticides have been found to widely induce positive effects on numerous organisms (3 Pharmaceuticals, 4 Microplastics
Conclusions and the way forward
Sub-NOAEL responses lead to positive outcomes such as enhanced ‘coping’ skills, stimulated growth, increased biomass, yields, and survival, extended lifespan, and improved reproduction, among others. They also lead to negative outcomes such as enhanced pathogenicity of pathogenic microbes, stimulation of weeds and pest insects, spread and development of resistance in weeds, insects, and microbes, and potential negative multi- or trans-generational effects. More studies are needed to address
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. E.A. acknowledges multi-year support from The Startup Foundation for Introducing Talent of Nanjing University of Information Science & Technology (NUIST), Nanjing, China (Grant No. 003080). E.J.C. acknowledges longtime support from the US Air Force (Grant No. AFOSR FA9550-13-1-0047) and ExxonMobil Foundation (Grant No. S18200000000256). The views and conclusions contained
CRediT authorship contribution statement
E.A. reviewed the literature, extracted data, created display elements, drafted the manuscript, had a leading role, served as the hub of communication among the authors, and supervised the production of the manuscript. D.B., J.R., C.S., E.J.C., and T.K. reviewed the manuscript and contributed intellectual input. All authors approved the final version for publication.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgement
The authors are grateful to Dr. Lei Yu of the Northeast Forestry University, Harbin, China, for comments on an early draft of the manuscript.
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