Hormesis induced by silver iodide, hydrocarbons, microplastics, pesticides, and pharmaceuticals: Implications for agroforestry ecosystems health

Highlights

• AgI, hydrocarbons, pesticides, pharmaceuticals, and microplastics induce hormesis.

• Sub-threshold doses induce positive and negative effects.

• Pathogenic microbes, weeds, and pest insects are stimulated.

• Their resistance to drugs is also facilitated.

• Sub-threshold effects hamper the achievement of Sustainable Development Goals.

Abstract

Increasing amounts of silver iodide (AgI) in the environment are expected because of the recent massive expansion of weather modification programs. Concurrently, pharmaceuticals, microplastics, hydrocarbons, and pesticides in terrestrial ecosystems continue contaminating forests and agroforests. Our review supports that AgI induces hormesis, a biphasic dose response characterized by often beneficial low-dose responses and toxic high-dose effects, which adds to the evidence for pharmaceuticals, microplastics, hydrocarbons, and pesticides induced hormesis in numerous species. Doses smaller than the no-observed-adverse-effect-level (NOAEL) positively affect defense physiology, growth, biomass, yields, survival, lifespan, and reproduction. They also lead to negative or undesirable outcomes, including stimulation of pathogenic microbes, pest insects, and weeds with enhanced resistance to drugs and potential negative multi- or trans-generational effects. Such sub-NOAEL effects perplex terrestrial ecosystems managements and may compromise combating outbreaks of disease vectors that can threaten not only forest and agroforestry health but also sensitive human subpopulations living in remote forested areas.

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.