Abstract
Herbicides play a crucial role in modern agriculture by controlling weeds and ensuring sustainable crop productivity. However, the use of herbicides has raised concerns regarding their contamination, posing serious threat to the environment, biodiversity, and food safety. Recent trends indicate a decline in the overall volume of herbicides usage, suggesting a shift towards more specific and targeted formulations of herbicides. Also, there has been an increased use of systemic and pre-emergence herbicides. The global agriculture still faces several challenges because of the adverse environmental impacts caused by herbicide contamination, both at the application site and offsite. In view of the growing concern, it is necessary to develop new herbicides with greater selectivity or bio-based herbicide that can degrade after successful control of the intended weed population and minimize or eliminate the environmental hazards. Furthermore, the adoption of integrated weed management practices rather than prolonged and repeated use of herbicide in agriculture can effectively reduce the growth of herbicide-resistant weed populations. The present review is a single valuable resource, providing insights into the recent trends and future challenges associated with herbicide use in modern agriculture, with a focus on human health and food safety. Also, we emphasize the advancements in herbicide technology, emergence of new herbicide-resistant weed species, regulatory considerations, and alternative approaches in herbicide use, all of which are particularly valuable to agroecology, policymakers, and stakeholders.
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Introduction
The global population is expected to reach 9.20 billion by 2050, necessitating a 70% increase in agricultural productivity to ensure food security (Kagan 2016). According to the Food and Agriculture Organization (FAO 2001), approximately 50% of usable land worldwide is dedicated to agriculture. Within this cultivable land, farmers encounter various challenges, including weeds, insects, and fungal infestations, of which, weeds pose a significant obstacle to agricultural productivity (Curran 2016). Weeds in farmland compete with the crops for nutrients, space, light, and moisture, leading to a reduction in production ranging from 20 to 50%, depending on their intensity and duration in the field (Kaur et al. 2019). Different methods are employed to control weeds, such as manual or mechanical and chemical approaches (Rose et al. 2016). By far, chemical control has become the preferred and effective method of weed management in view of labor costs and the need for quick weed control and enhanced agricultural productivity with reduced cost (Sondhia 2014; Janaki et al. 2015). Consequently, herbicide application has become an integral part of modern agriculture, playing a crucial role in increasing production and keeping non-crop areas free from weeds (Cobb 2022). Currently, over 4.10 million tons of pesticides are consumed globally, with herbicides accounting for 47.50 followed by insecticides (29.50%), fungicides (17.50%), and others (5.50%) (Sharma et al. 2019a; Riedo et al. 2021). Since 1945, agricultural farmers in both developed and developing countries used more than 200 active ingredients of herbicides for weed management, accounting for over 25% of total pesticide consumption during the past decade (Green 2014). This growth in agrochemical production and consumption has been driven by robust economic expansion, including the agricultural and industrial sectors, particularly in the late nineteenth century (Sharma et al. 2019a).
Despite their role in increasing crop yields and ensuring food security, herbicides pose significant risks to human and environmental health due to the occurrence of these hazardous compounds in various environmental settings (Fernandes et al. 2020). When herbicides are applied in agricultural fields, urban areas, and forests, they can adversely affect both short- and long-term, humans, animals, insects, wildlife, and fish (Khan et al. 2023). Additionally, improper and excessive herbicide use can result in residues in plants and soils, crop toxicity, development of herbicide-resistant weeds, and harmful effects towards nontarget organisms (Sondhia 2014; Janaki et al. 2015). The consumption of agrochemicals poses significant hazards due to the proximity between humans and the environment (Cioffi et al. 2021). Inappropriate handling of herbicides in farmlands can significantly impact crop, animal, and human health, while nontarget organisms can also be at risk due to herbicide residues entering the food chain (Singh and Singh 2016). The offsite migration of herbicides to surface water through runoff, leaching to groundwater, and volatilization into the air has detrimental effects towards nontarget organisms (Andreu and Picó 2004). Indeed, residues of persistent herbicides persist in crops, soil, water, and air for extended periods, posing potential hazards to human and environmental health (Sharma et al. 2019b). Given the intensive use of various herbicides in agriculture, it is crucial to determine the residues in different environmental settings to understand their overall fate and behaviour, which is greatly warranted for implementing effective risk management strategies (Meftaul et al. 2020).
During the last decade, there has been a significant shift towards input-intensive agriculture. Various developments and strategies have emerged, including increased efforts by the agrichemical industry in discovering new herbicides, the adoption of genetically modified herbicide-resistant crops, breeding for weed-competitive crop cultivars and a greater reliance on systemic and new generation of pre-emergence herbicides (Beckie et al. 2019). These systemic and pre-emergence herbicides play crucial roles in modern agriculture and weed management strategies. Systemic herbicides are absorbed by plants and move through their vascular systems, effectively targeting weeds from the inside out, offering broad-spectrum control and efficiency (Amna et al. 2019). In contrast, pre-emergence herbicides, applied before weed growth, can prevent weed species from germinating, reduce competition with crops and ensure higher yields (Oliveira et al. 2020). Also, it minimizes the need for post-emergence herbicides, reducing overall chemical usage and environmental impact. Furthermore, recent trends indicate a decline in the overall volume of broad-spectrum herbicides used, accompanied by a shift towards more specific and targeted formulations (Damalas and Koutroubas 2018). These targeted formulations are designed to specific weeds or unwanted vegetation while minimizing harm to desired plants thereby reducing the overall amount of chemicals needed for effective weed control. One of the most notable changes in global herbicide-resistant weed management strategies has been the increased emphasis on reducing the weed seed bank and maintaining low seed bank levels through any possible means (Beckie et al. 2019). The evidence mounting on the adverse effects of agrochemicals on the environment and human health necessitates a transition from the productivity-focused approach to sustainable and eco-friendly agriculture. Still, it is crucial that herbicides are formulated in a manner that allows them to degrade from the environment after fulfilling their intended purposes (Janaki et al. 2015; Sondhia 2014). The fate, ecological effects of herbicides and their residues have not been thoroughly understood in agricultural soils, and information available in the literature concerning the upcoming challenges in herbicide use for sustainable agriculture and food security is very limited and fragmentary. Therefore, this review is the first single source that aims to update and consolidate the existing literature in this research area by highlighting the emergence of new herbicide-resistant weed species, recent trends in herbicide use, developments in herbicide technology, regulatory considerations, and future challenges in developing alternative approaches of herbicide usage to ensure food security and safety, all of which are predominantly valuable for farmers, consumers, policymakers, and industry stakeholders.
Importance of herbicides in modern agriculture
Weeds are considered as a major obstacle in the modern farming system, as they reduce crop yield and quality, resulting in many billion dollars of crop losses annually (Abouziena and Haggag 2016). It is well documented that the losses caused by weeds have exceeded those from any category of agricultural pests, viz., insects, diseases, nematodes, rodents, etc. (Oerke 2006). Rao (2000) reported that the total annual losses of agricultural produce from weeds, insects, diseases, and other pests account for 45, 30, 20 and 5%, respectively. Globally, the estimated damage caused by weeds is around US $40 billion per year (Abouziena and Haggag 2016), which is over $26 billion in the USA alone, causing a major threat to food security (Délye et al. 2013). Consequently, herbicide use is the best way of controlling weed infestation in the agricultural farming system, offering easy application coupled with economic sustainability (Singh et al. 2020), quick action and efficient killing of approximately 90–99% of the targeted weeds (Délye et al. 2013). During the last century, herbicides became an unavoidable tool of agriculture, which allowed for a noticeable increase in crop yield to feed a rapidly growing human population (Carvalho 2017). Accordingly, global herbicide consumption has drastically increased by many folds, contributing to 47.50% of the total pesticide usage (Singh et al. 2020). Nearly, two thousand herbicide compounds have been discovered and put into application for the management of weeds in different arable lands worldwide. It may either be applied to the soil during land preparation or directly to the foliage (Sherwani et al. 2015).
Pre-emergence herbicides are applied to the soil surface to kill weeds before the seedling emergence (Preisler et al. 2020). Examples of pre-emergence herbicides include imazethapyr, isoxaflutole, metolachlor, and pendimethalin (Mobli et al. 2020). Post-emergence herbicides are applied to weed seedlings that have already emerged and 2,4-D, imazethapyr, imazamox, and metribuzin are examples of post-emergence herbicides (Taran et al. 2013). The diversified groups of herbicides (Table 1) help to eradicate different weed species without disturbing crop plants (Vats 2015). Herbicides can also be classified based on their mechanism of action and chemical family. The mode of action refers to the specific biochemical or physiological process targeted by the herbicide (Fig. 1), while the chemical family represents the structural similarity among herbicides. A detailed classification based on the mode of action and chemical class is provided in Table 2. Also, herbicides are widely used as plant growth regulators in crops, gardens, and lawns (Sack et al. 2015). For instance, lower amounts of glyphosate can stimulate plant growth (the effect is termed hormesis), helps to ripen sugarcane and inhibits rust diseases in glyphosate-resistant wheat and soybean (Velini et al. 2010). In recent years, farmers rely more on herbicides in agricultural farming due to increased labour wages and sometime unavailability of agricultural labour. Thus, herbicides became a crucial component for controlling undesirable noxious weeds in modern agriculture.
Recent trends in weed management
Recent trends in herbicide usage have been a subject of significant interest in the agricultural community over the past decade. However, the mode of action and human and environmental health effects of the formulations differ based on the chemical groups (Özkara et al. 2016). The recent trends in herbicide usage suggest a gradual decline in the overall volume of herbicides, accompanied by a shift towards more specific and targeted herbicide formulations (Damalas and Koutroubas 2018; Cech et al. 2022). This shift is largely attributed to increased awareness of the potential ecological and health risks associated with indiscriminate herbicide application (Devi et al. 2022). Additionally, advancements in precision agriculture technologies have played a crucial role in facilitating more efficient and targeted herbicide use (Kendall et al. 2022). These findings provide valuable insights for farmers, policymakers, and industry stakeholders, aiding in the development of sustainable herbicide management strategies that balance weed control efficacy with environmental concerns (Li et al. 2020; Kendall et al. 2022).
Increased application of systemic herbicides
Nowadays, systemic herbicides have gained popularity due to their effectiveness in controlling weeds (Tsai 2019). For instance, glyphosate is a systemic herbicide that has been widely used in agriculture for several decades due to its effectiveness against a wide range of weed species in various crop systems (Green 2009; Gage et al. 2019). However, concerns have been raised regarding the development of glyphosate-resistant weeds, prompting the need for alternative herbicides and management strategies (Duke and Powles 2009). Also, dicamba and 2,4-D has gained attention for its use as systemic herbicide to control broadleaf weeds in crops of soybean (Glycine max L.), cotton (Gossypium hirsutum L.), and genetically modified 2,4-D- and dicamba-tolerant soybeans in various agricultural and non-agricultural settings (Gage et al. 2019). However, dicamba has faced regulatory challenges and concerns about off-target movement, leading to restrictions on its use in some regions. Like dicamba, 2,4-D has been associated with concerns related to off-target movement and potential damage to sensitive crops and vegetation. Glufosinate is a non-selective systemic herbicide used primarily to control weeds in herbicide-tolerant crops of corn, soybeans, and cotton, and has gained popularity as an alternative to glyphosate in some cases (Sammons and Gaines 2014). However, the emergence of glufosinate-resistant weeds is a troubling issue that warrants careful attention and management strategies. As modern agriculture continues to evolve, it is necessity to address these challenges through innovative herbicide management strategies and explore sustainable alternatives to ensure the long-term efficacy of weed control in various crop systems.
Increased use of pre-emergence herbicides
In recent years, there has been a noticeable shift in usage towards pre-emergence herbicides. Pre-emergence herbicides are applied to the soil before the crop emerges, targeting weed seeds and seedlings in the soil, and these herbicides can effectively suppress weed growth before they emerge, and provide better weed control compared to post-emergence herbicides (Cioni and Maines 2010). This trend has gained traction due to several advantages offered by pre-emergence herbicides, such as increased effectiveness, reduced herbicide resistance, preventing weed from competing with crops for nutrients, water and light, and improved crop safety (Zimdahl 2018). Furthermore, herbicide resistance is a major concern in modern agriculture, where weeds develop genetic resistance to commonly used herbicides, by incorporating pre-emergence herbicides into weed management strategies, farmers can diversify their herbicide modes of action, reducing the risk of herbicide resistance development and preserving the efficacy of herbicides for longer periods (Cioni and Maines 2010; Gage et al. 2019).
Pre-emergence herbicides are typically applied before the crop has emerged and this timing allows for better selectivity, as the herbicide can be targeted to the soil where weed seeds are present, minimizing contact with emerging crop plants, which reduces the risk of crop injury and enhances overall crop safety (Cioni and Maines 2010; Zimdahl 2018). Several pre-emergence herbicides have gained prominence in agricultural practices, and these include Group 14 herbicides (such as sulfentrazone and flumioxazin) and Group 15 herbicides (like acetochlor, metolachlor, and S-metolachlor), which effectively control both broadleaf weeds and grasses in crops of corn, soybeans, cotton, and peanuts (Umphres et al. 2018; Brabham et al. 2019; Rangani et al. 2021; Wang et al. 2021). In addition, Group 5 herbicides (such as metribuzin and flumioxazin) are employed for broad-spectrum weed control in crops like potatoes, soybeans, and peas (Ali et al. 2020; Hutchinson 2020) whereas Group 3 herbicides (like pendimethalin and trifluralin) exhibit selectivity in controlling grassy weeds and are widely used in various crops, including corn, wheat, and several vegetables (Chhokar et al. 2012; Parween et al. 2016). Therefore, the pre-emergence herbicides of Group 3, Group 5, Group 14, and Group 15 have become integral components of weed management in different crop types, ensuring efficient control of both broadleaf weeds and grasses.
Use of genetically modified herbicide-resistant crops
The phenomenon of adopting genetically modified (GM) herbicide-resistant crops has emerged as a prominent trend in herbicide usage within the agricultural sector over the past few decades (Meftaul et al. 2020). These crops are genetically engineered to tolerate specific herbicides, allowing farmers to control weeds more effectively while minimizing damage to the cultivated crops (Duke and Powles 2008; Owen et al. 2015). Notably, glyphosate-resistant crops such as soybeans, corn, cotton, and canola have gained widespread acceptance among farmers globally (Duke and Powles 2008). The introduction of glyphosate-resistant crops has led to increased reliance on glyphosate-based herbicides, like Monsanto's Roundup® (Belz and Duke 2014). The glyphosate-resistant crops have provided farmers with more flexibility and convenience in weed management, resulting in enhanced crop yields and reduced labor costs. Apart from glyphosate resistance, crops with resistance to other herbicides have also been developed and commercialized. For example, crops engineered to tolerate herbicides like glufosinate, 2,4-D, and dicamba have gained adoption in various regions (Shaner 2014). These herbicide-resistant crops provide farmers with additional options for weed control and help manage herbicide resistance by rotating the use of different herbicides (Gaines et al. 2010). The adoption of GM herbicide-resistant crops has provided several benefits to farmers, including improved weed control, increased crop yields, and reduced tillage (Powles and Yu 2010). However, there are concerns related to herbicide-resistant weed evolution and the potential environmental impact of increased herbicide use (Heap 2019). The overreliance on a single herbicide or herbicide mode of action can lead to the selection of herbicide-resistant weed species, necessitating integrated weed management strategies (Powles and Yu 2010). The adoption of GM herbicide-resistant crops has undoubtedly transformed weed management practices in agriculture. However, it is essential to implement sustainable and integrated approaches to mitigate the challenges associated with herbicide resistance and environmental impacts, ensuring long-term food security, safety, and sustainability.
Herbicide resistance in weeds
Emergence of herbicide-resistant weed species
Globally, weed resistance to herbicides (Table 3) is ever-growing and is alarming for global food security (Délye et al. 2013). The continuous and long-term use of the same herbicide(s) with the same mechanism of action leads to changes in the weed population, and makes them resistant (Qasem 2011). For example, after the introduction of genetically modified (GR) herbicide resistance (HR) crops, the repeated and prolonged application of glyphosate over the past few decades has led to the emergence of resistance in certain weed species (Gage et al. 2019). Over time, resistant weeds reproduce successfully and become dominant in the population (Bo et al. 2017). The development of herbicide resistance is influenced by various factors, including herbicide chemistry, application rate, and non-chemical factors (Renton et al. 2014). The first reported case of herbicide resistance occurred in 1957, when wild carrot (Daucus carota L.) developed resistance to the herbicide 2,4-D in Canada, and since then, over two hundred weed species worldwide have been reported to develop resistance to one or more herbicides (Délye et al. 2013). The highest number of herbicide-resistant weeds has been recorded in the USA (144), followed by Australia (62), Canada (59), France (35), and China (34) (Heap 2014). Herbicide resistance was not initially expected to be a significant problem before 1960; however, the discovery of common groundsel (Senecio vulgaris L.) weed population resistant to simazine or atrazine in 1968 raised concerns among the scientific community (Shaner 2014; Moss 2017). Examples of herbicide-resistant weeds include wild radish (Raphanus raphanistrum L.) in Australia, which developed resistance to 2,4-D and MCPA, prickly lettuce (Lactuca serriola L.) in the USA, resistant to 2,4-D, MCPA, and dicamba, and corn poppy (Papaver rhoeas L.) in Europe, resistant to phenoxy herbicides (Busi et al. 2018a). Glyphosate-resistant (GR) crops were commercially introduced in North and South America in 1996 (Shaner 2014). However, glyphosate resistance developed in different weed species due to repeated and continuous application of glyphosate (Fernández et al. 2017). The first glyphosate-resistant weeds were observed in Lolium rigidum in 1996 and Eleusine indica in 1997, after its frequent applications (5 to 10 times per year) for more than 15 years (Heap 2014). So, herbicide-resistant weeds continue to increase and pose a significant threat to crop production worldwide, affecting desirable plants and animals (Peterson et al. 2018).
Mechanisms of herbicide resistance
In modern agriculture, herbicide resistance poses a major challenge by diminishing the effectiveness of herbicides in controlling weed populations (Peterson et al. 2018). Studies revealed that several key mechanisms and causes contribute to herbicide resistance, and one such mechanism is target-site resistance (for example, resistance to ACCase inhibitor, ALS inhibitor, and PSII inhibitor), which occurs when genetic mutations in the target protein or enzyme responsible for herbicide binding or activity make it less susceptible to the herbicide's mode of action (Heap 2014; Moss 2017). These mutations can either arise spontaneously or through repeated exposure to herbicides. For instance, the target-site resistance mechanisms include altered target-site proteins, target-site gene amplification, and target-site overexpression (Heap 2014; Moss 2017). On the other hand, metabolic resistance is another type of resistance in which the weed enhances the metabolism or detoxification of herbicides, thereby reducing the concentration or activity of the herbicide within the plant (Yu and Powles 2014). This resistance is attributed to the overexpression or altered function of cytochrome P450 monooxygenases, glutathione transferases, or esterases, all involved in herbicide metabolism (Yu and Powles 2014). Weeds can also develop resistance by restricting herbicide uptake or translocation within the plant, thereby reducing the herbicide's effectiveness (Gressel 2015). The reduced uptake or translocation can result from changes in membrane permeability, the presence of active efflux transporters, or impaired translocation processes (Gressel 2015; Busi et al. 2018b). Furthermore, multiple resistance occurs when weeds exhibit resistance to more than one herbicide, often due to the accumulation of different resistance traits in a weed population or the horizontal transfer of resistance genes between species (Busi et al. 2017). Therefore, to successfully manage weed species that have developed resistance, it is crucial to understand the underlying mechanisms and causes of such resistance.
Environmental implications of herbicide use in modern agriculture
The environmental toxicity of herbicides is influenced by several factors, including the physicochemical properties of the herbicides, soil conditions, meteorological factors, application methods, frequency and quantity of use, and the biotic and abiotic characteristics of the environment (Tsai 2013; Fingler et al. 2017). Furthermore, the use of additives/adjuvants in combination with herbicide active ingredient can increase their toxicity to the surrounding environment and nontarget plants and animals (Gandhi et al. 2021). While adjuvants can enhance the performance of herbicides, they can also contribute to the formation of persistent residues in soil and plants, leading to potential adverse effects. For instance, the residue formation of trifluralin in soil and sugar beet roots was found to be higher ranging from 42 to 49% when adjuvants were used (Pacanoski 2015). The extensive use of herbicides also results in their accumulation in the environment, particularly in aquatic systems near agricultural areas, further contributing to toxicity concerns. Therefore, it is crucial to monitor the fate and behavior of herbicides in agricultural soil to assess their toxicity and minimize negative impacts on ecosystems (de Castro et al. 2017). Overall, Fig. 2 depicts the fate and movement of herbicides in diverse sections of the environment, while Table 4 presents the related data.
Mobility of herbicides in the environment
Herbicides can also spread from agricultural areas to other parts of the environment through spray drift, volatilization, runoff, and leaching, which can have detrimental effects on nontarget organisms as well as human and environmental health (Schreiber et al. 2018; Ramakrishnan et al. 2019). It has been shown that only 45% of the sprayed herbicides reach the target plants, while 30% is drifted, 10% is lost by runoff, leaching, and volatilization processes, and 15% reaches soil (Schreiber et al. 2018). The horizontal running of herbicides that are dissolved in water or adsorbed with eroding soil over a sloping surface is called surface runoff (Tiryaki and Temur 2010; Kanissery et al. 2020). In fact, the amount of runoff significantly depends on topography, soil texture, soil moisture content, herbicide formulation, climatic conditions, and management practices (Tiryaki and Temur 2010; Delcour et al. 2015). On the other hand, the mobility of herbicides in soil by water to a downward direction is known as leaching, which poses a potential threat to groundwater contamination (Kanissery et al. 2020). The characteristics of herbicides and soil, and their interaction with water from irrigation or rainfall, climatic conditions, and geography play a vital role in leaching (Tiryaki and Temur 2010). Also, leaching can be increased when the soil is sandy or the herbicide is water-soluble if rainfall occurs soon after spraying, and the herbicide is not strongly sorbed to the soil (Tiryaki and Temur 2010). Consequently, the weed-control efficiency, particularly pre-emergent herbicides, may decline (Kanissery et al. 2020). If runoff, which depends mostly on the addition of water (rainwater and irrigation water) to a field, is faster than the sorption of herbicides to soil, > 5% of the total applied chemical is lost that contaminates the environmental surface waters (Tiryaki and Temur 2010). Another most important transformation route of herbicides is volatilization, which occurs through evaporation from soil and plant material followed by dispersion into the aerial atmosphere by diffusion and turbulent mixing (Prueger et al. 2005) and later deposited in streams, rivers, and lakes (Thurman and Cromwell 2000; Kuang et al. 2003). Several factors affect herbicide volatilization from the soil, including the soil moisture content, herbicide's vapor pressure, sorption, water-solubility, soil texture, weather conditions, and size of spray drops (Tiryaki and Temur 2010; Blasioli et al. 2011). For instance, wet and sandy soils, hot, windy, or dry weather, and small spray drops increase volatilization of herbicides from soil to the atmosphere (Tiryaki and Temur 2010). Eventually, the volatilization of herbicide increases the risk of contaminating the atmosphere and consequently affecting nontarget organisms (Schreiber et al. 2018). In addition, other organic contaminants like PAHs and volatile contaminants can also move long distances and accumulate in soil, posing long-term health risks (Ambade and Sethi 2021; Ambade et al. 2023). Climate change leads to rising temperatures and decreasing rainfall trends over time, causing adverse effects on agriculture (Meshram et al. 2018, 2020). Thus, developing sustainable weed management strategies along with adopting sustainable resource management practices is crucial to address environmental challenges (Javan et al. 2023; Sabah et al. 2023; Suseno and Basrowi 2023).
Persistence/degradation of herbicides in the environment
The persistence of herbicides or other agrochemicals in soil, plants, water, and the air is a raising global concern. Herbicides are considered persistent when they remain in soil long after their intended use, entering plants and potentially causing food toxicity (Helling 2005). The repeated application of the same herbicides contributes to their persistence due to slow degradation (Basu and Rao 2020). Herbicide persistence is measured by its half-life (DT50), which represents the time it takes for 50% of the original quantity applied to break down in the soil (Helling 2005). Based on their relative persistence, herbicides can be categorized as long-lasting (> 6 months), moderate (3‒6 months), low (1‒3 months), or non-persistent (< 1 month) (Basu and Rao 2020). Long-lasting herbicides have a higher potential to spread in different parts of the environment through surface water and groundwater (Basu and Rao 2020). Herbicide residues tend to be less persistent on vegetation and plant canopies than in soil (Tiryaki and Temur 2010). But persistent herbicides can still pose a significant risk to human health when found in soil, surface, and groundwater, surrounding environments, and agricultural products (Qasem 2011). Therefore, it is crucial to avoid the use of persistent chemicals unless there are no alternative options and only when necessary. Triazines, sulfonylureas, uracils, bipyridiliums, phenylureas, dinitroanilines, imidazolinones, isoxazolidiones, and some plant growth regulators (Table 5) are known for their persistence (Janaki et al. 2015; Curran 2016).
In contrast, degradation is the major route of herbicide breakdown and reduce the concentration from soil and the environment (Kanissery et al. 2020). Generally, degradation of herbicides occurs by biotic (via soil microorganisms) and abiotic (i.e., degradation by sunlight or chemical) processes (Lourencetti et al. 2012; Kanissery et al. 2020). Soil microorganisms (bacteria, fungi, and protozoans) facilitate biodegradation through metabolic or enzymatic process (Kanissery et al. 2020), which is the most crucial pathway responsible for the breakdown of herbicides (Curran 2016). These organisms utilize herbicides and organic matter or other substances as a source of energy and carbon (Tiryaki and Temur 2010), whereas some herbicides act as good sources of carbon and/or nitrogen for soil microorganisms (Kanissery and Sims 2011). The rate of biodegradation is proportional to microbial activity in soil, which is higher in areas with high organic matter, particularly in the soil surface horizons, and warm, humid, and well-aerated soil conditions (Tiryaki and Temur 2010). When microbial activity decreases in extremely alkaline or acidic soil, abiotic degradation or chemical degradation will be rapid (Tiryaki and Temur 2010), which occurs through oxidation–reduction, hydrolysis, and ionization reactions in soil (Kanissery et al. 2020). Photodegradation is another abiotic process of herbicide breakdown from soil surfaces, plant foliage, air, and water by the ultraviolet radiations of sunlight (Blasioli et al. 2011; Kanissery et al. 2020). Most of the herbicides are susceptible to photodegradation due to the presence of aromatic ring structures, heteroatoms, and other functional groups (Orellana-Garcia et al. 2014). Generally, the photolysis process is slower in water than in soil, and direct photolysis will occur within a shallow surface zone, approximately 0.20–0.30 mm vertical depth of soil (Konstantinou et al. 2001). Several factors affect the degradation of herbicides in soil, including soil properties like texture, organic matter content, pH, and microbial community, herbicide chemistry (solubility, log Kow, vapor pressure, half-life, and log Koc), climatic factors (temperature, rainfall, and aeration), and vegetation (Helling 2005). For example, no or minimal soil microbial activity results in persistence of glyphosate for up to 200 days in soils (Kanissery et al. 2020).
Food safety concern of herbicide residues
There are several issues associated with herbicide use, including overuse, improper application, incorrect selection, and harvesting crops immediately after herbicide application, which can result in higher levels of chemical residues in foods consumed by consumers (Handford et al. 2015; Meftaul et al. 2023). Depending on the level of exposure, these herbicide residues can have potential adverse effects on human health (Handford et al. 2015). Since food is a significant pathway for herbicide residues to enter the human body, it is crucial to monitor residue levels in food to ensure food safety (Zhang et al. 2015; Su et al. 2018). Most countries regulate pesticides using MRLs, which define the highest allowable amount of pesticide residue in food and feed when pesticides are correctly applied following Good Agricultural Practice (Handford et al. 2015; Wanwimolruk et al. 2015). Several countries, including Australia, India, Greece, China, Korea, Japan, Spain, etc., monitor pesticide residue levels in fruits, crops, and vegetables (Hasan et al. 2017). Plants can easily absorb residues from the soil, water, and air, transferring them through the food chain. For instance, herbicide residues were found to exceed MRLs in 6.60% of cereal samples in India (Sondhia 2014). Samples of food crops in Korea showed residues of 2,4-D at a concentration of 0.102 mg kg‒1, whereas 0.023‒0.26 mg kg‒1 levels of glyphosate were detected in spinach and lettuce, respectively, grown in backyard garden soil in Australia (Shin et al. 2011; Meftaul et al. 2023). In Nigeria, crops of cassava, yam, potato, and groundnut had higher average concentrations of herbicide residues compared to leafy vegetables, with atrazine, 2,4-D, and paraquat occurring at 0.04, 0.02, and 0.67 mg kg‒1, respectively (Gushit et al. 2013).
If herbicides are applied close to the harvest date, large amounts of residues may be found in crops. For example, when pre-harvest Roundup was applied, glyphosate residues were found in two wheat varieties Major (11.10 mg kg‒1) and Walton (6.10 mg kg‒1) that are above the MRLs set by Health Canada (Xu et al. 2019). Diuron can persist in the environment for a long time and transfer trace amounts of residues to humans through the food chain, potentially affecting human health (Su et al. 2018). Since many fruits and vegetables are consumed raw, the possibility for the presence of pesticide residues in them is higher than in other crops (Stachniuk et al. 2017). However, even small amounts of herbicide residues in daily diets can lead to long-term health problems, including acute, chronic, or sub chronic difficulties (Gómez-Ramos et al. 2020). Consumers are already rejecting the use of hazardous chemicals in crop production to avoid chemical residues in food and ensure clean and safe consumption (Carvalho 2017). Therefore, to safeguard consumer health and ensure food safety, it is essential to follow good agricultural practices (GAP) and continuously monitor herbicide residues to essure food safety and minimize environmental health hazards (Prodhan et al. 2018).
Human health effects of herbicides
Human exposure to herbicides and health risks
The impact on human health associated with herbicide exposure is influenced by factors like the type of herbicide, dosage, exposure routes, and duration of exposure (Marin-Morales et al. 2013). Exposure to herbicides can occur through direct contact and inhalation in agricultural areas or indirectly through consumption of contaminated food and water (Anderson and Meade 2014), leading to acute and chronic health effects (Table 6). Prolonged exposure to herbicides can result in different types of cancer, neurodegenerative disorders, developmental and reproductive changes, and respiratory effects (Marin-Morales et al. 2013). For instance, glyphosate-based herbicides have been associated with endocrine disruption, liver and kidney damage, DNA damage, reproductive problems, and various neurodegenerative disorders (Thongprakaisang et al. 2013; Séralini et al. 2014; Kwiatkowska et al. 2017). Residues of glyphosate and its metabolite, AMPA, which can be found in water and agricultural products, are consumed by humans, and excreted through urine (Maheswari and Ramesh 2019). Similarly, atrazine herbicide contamination in drinking water has been linked to an increased risk of breast cancer in women, lower sperm counts in rural men, and decreased birth weight in children (Sankhla et al. 2018).
Another highly toxic herbicide, paraquat, with a lethal dose of 30 mg kg‒1 poses serious risks to human health, causing vomiting, nausea, diarrhea and fluid, and electrolyte loss upon ingestion (Tsai 2013). Acute exposure to paraquat through ingestion, inhalation, or dermal contact can lead to damage of heart, kidneys, liver, adrenal glands, muscles, and spleen as well as central nervous system, potentially resulting in multiple organ failure and death within 24 h. Dermal exposure to paraquat can cause dermatitis and skin burns, while accumulation in the lungs and kidneys has been associated with gall bladder cancer, lung cancer, and stomach cancer (Tsai 2013; Delirrad et al. 2015). Exposure to 2,4-D, 2,4,5-T, and MCPA can result in abdominal pain, vomiting, diarrhea, hypertension, headache, and gastrointestinal haemorrhage (Bradberry et al. 2000; Islam et al. 2018). Dermal or inhalational exposure to 2,4-D can cause skin irritation, itching, and breathing difficulties (Islam et al. 2018). The presence of 2,4-D has been detected in the urine samples of pregnant women (120 μg L‒1) and children (2.90 µg L‒1) living near farms in Ontario, Canada, indicating their potential exposure, and has been linked to respiratory cancers, gall bladder cancer, and pancreatic cancer among farmers and factory workers (Islam et al. 2018). The herbicide pendimethalin caused toxicity in applicators and their spouses, and its ingestion can lead to gastrointestinal damage, including nausea and epigastric pain (Arici et al. 2020). Long-term exposure to pendimethalin has been associated with an increased risk of rectal cancer, pancreatic cancer, and lung cancer among applicators (Mostafalou and Abdollahi 2013; Arici et al. 2020). Non-selective and non-biodegradable herbicides are particularly toxic and can persist in the environment for extended periods, posing a significant risk to humans and animals (Marin-Morales et al. 2013; Gupta 2018). Indiscriminate use or improper disposal of herbicide containers contributes to excessive herbicide exposure, resulting in more than one million deaths and numerous chronic diseases worldwide (Zhang et al. 2015; Gupta 2018).
Potential toxic effects toward other non-target organisms
The environmental impact of herbicides extends to nontarget organisms, including soil microorganisms, aquatic species, insects, birds, and other animals (Zhao et al. 2013). For example, glyphosate, has been found to negatively impact a wide range of organisms, from arthropods, fishes, reptiles, molluscs, amphibians, and birds (Gill et al. 2018). Glyphosate concentrations above 10 mg L‒1 have been observed to hinder the growth of beneficial mycorrhizal fungi (Thelephora americana, T. terrestris, Suillus tomentosu, and Hebeloma crustuliniforme) and adversely affect earthworms, with reduced multiplication rates, DNA damage, loss of biomass, and diminished casting activity (Freemark and Boutin 1995; Gill et al. 2018). Bees, vital for pollination in both agricultural and wild plant species, are also negatively impacted by glyphosate (Belsky and Joshi 2020). The commercial formulation of glyphosate containing surfactant, polyethoxylated tallowamine (POEA) can be more toxic to terrestrial and aquatic animals as compared to pure glyphosate (Gandhi et al. 2021).
The long-term application of atrazine and 2,4-D can have detrimental effects on soil microorganisms, nitrogen-fixing bacteria, and enzyme production in soil (Rose et al. 2016). 2,4-D has adverse impact on the reproduction and development of earthworms and reduce the nitrogenase, phosphatase and hydrogen photoproduction activities of Rhizobium species and purple non-sulphur bacteria (Correia and Moreira 2010; Meena et al. 2020). Fish species (Rhamdia quelen) exposed to 2,4-D exhibited altered behavior, including lethargy and erratic swimming (de Castro et al. 2017). Dicamba, 2,4-D, and paraquat exerted high toxicity towards beneficial insects (Bohnenblust et al. 2016). The larvae of ladybird beetle (Coleomegilla maculate) are particularly vulnerable to the commercial formulation of 2,4-D, while dicamba decreased body weight and increased mortality (Freydier and Lundgren 2016). Indirect effects of herbicides pose a higher risk to habitats neighboring agricultural fields as compared to direct effects (Prosser et al. 2016). By reducing food sources of birds such as insects and grains, herbicides contribute to a decline in bird species in agricultural areas (Boatman et al. 2004). Further research is necessary to understand the fate and effects of newly released herbicides that are frequently used in agroecosystems. Figure 3 depicts the overall potential detrimental effects associated with the herbicide exposure to humans and other nontarget organisms.
Challenges and future research directions
Developing new herbicides with improved safety profiles
With growing concerns about the impact of herbicide residues on human and the environmental health, there is an urgent need to develop safer herbicides. Researchers are now focusing on developing herbicides that specifically target weed species while minimizing harm to nontarget organisms, which requires a deeper understanding of the molecular mechanisms underlying the weed growth to design herbicides that selectively inhibit these processes (Qu et al. 2021; Vasseghian et al. 2022). For instance, enzyme inhibitors and receptor-based herbicides offer more precise weed control to reduce the ecological impact, and it is crucial to develop herbicides that break down rapidly or firmly bind to soil particles, preventing their movement into groundwater or surface water (Casida and Durkin 2017; Qu et al. 2021). This can be achieved with biodegradable herbicides or formulations that enhance soil adsorption. However, selective herbicides that effectively eliminate weeds without harming crops are highly desirable (Takano et al. 2020; Torra et al. 2021). Future research should also be directed to develop new herbicides with greater selectivity, allowing farmers to target specific weed species while minimizing damage to agricultural crops (Torra et al. 2021). This can be accomplished through the cultivation of herbicide-resistant crop varieties or the use of herbicides that exploit physiological differences between crops and weeds.
The discovery and development of herbicides with innovative modes of action are critical for overcoming resistance of weed species (Qu et al. 2021; He et al. 2022). Research efforts are currently focused on identifying new target sites within weeds and developing herbicides that disrupt their essential processes, which includes assessing natural products, bio-based herbicides (sustainable alternatives to synthetic herbicides), and plant extracts with herbicidal properties (Damalas and Koutroubas 2018). Furthermore, researchers are exploring the use of herbicide combinations or stacked herbicide traits in genetically modified crops (Vats 2015; Tsatsakis et al. 2017). By employing multiple herbicides with different modes of action, the risk of herbicide resistance can be minimized, and weed control effectiveness can be enhanced (Gage et al. 2019; Gaines et al. 2021). However, it is crucial to assess the potential synergistic or additive effects of these combinations on nontarget organisms and the environment. Future research should prioritize the improvement of methods for evaluating the environmental risks of herbicides, which involves assessing their impacts on soil health, water quality, beneficial organisms, and ecosystems. Developing standardized and robust testing protocols can facilitate the effective evaluation and regulation of new herbicides. Beyond the development of new herbicides, research should emphasize the promotion of sustainable weed management strategies which includes integrated weed management approaches that combine cultural, mechanical, biological, and chemical control methods. Implementing effective weed monitoring and decision support systems can optimize herbicide use and minimize environmental impacts.
Identifying sustainable weed management practices
The future of weed management poses several challenges that require research and innovative approaches. One crucial area to explore is the integration of multiple strategies, including cultural, biological, and chemical methods, to optimize effectiveness while minimizing the use of herbicides (Andrew et al. 2015; Bueno et al. 2021). Within an Integrated Weed Management (IWM) framework, it is essential to investigate the ideal combination and timing of different weed management techniques to maximize control and minimize herbicide resistance (Riemens et al. 2022). Advanced technologies can play a significant role in sustainable weed management. The development of remote sensing, drones, and machine learning can enable real-time detection and mapping of weed populations, facilitating targeted herbicide application (Sishodia et al. 2020; Ghatrehsamani et al. 2023). Additionally, site-specific weed management techniques like variable-rate herbicide application, can optimize control while reducing environmental impact (Gerhards et al. 2022).
To explore more natural and eco-friendly options, research should focus on identifying and utilizing natural enemies like insects, pathogens, and allelopathic plants for weed suppression (Mehdizadeh and Mushtaq 2020; Hasan et al. 2021). Bacteria and fungi hold potential for bioherbicide development, offering effective and environmentally friendly weed control alternatives (Duke et al. 2018; Hasan et al. 2021). Furthermore, studying the impact of cover crops and diversified crop rotations on weed suppression, soil health, and crop productivity are crucial to reduce the reliance on herbicides and promote sustainable farming practices (Blanco‐Canqui et al. 2015). Investigating the allelopathic potential of cover crops can provide a natural approach to inhibit weed germination and growth (Sturm et al. 2018). Preventing the replenishment of weed seed banks is another area of interest. For instance, strategies like seed predation by birds and insects, as well as seed burial through tillage practices, can be explored to minimize weed seed persistence (Saska and Honěk 2022). Techniques like seed dormancy-breaking and seedling recruitment prediction models can be developed to target weed seeds and prevent their establishment (Storkey et al. 2021). In terms of herbicides, the focus should be on developing formulations with enhanced selectivity, lower environmental persistence, and reduced off-target effects (Heap and Duke 2018). Exploring new herbicide formulations (nanoformulations) and delivery systems (microencapsulation), can improve efficacy and minimize environmental impact (Li et al. 2021). It is essential to evaluate the economic and social implications of sustainable weed management practices to ensure their practical adoption by farmers (Bergtold et al. 2019). Moreover, assessing and developing policy frameworks that incentivize the adoption of sustainable weed management practices can promote long-term food safety and environmental sustainability (Mango et al. 2017; Buddenhagen et al. 2022).
Enhancing public awareness on herbicide safety
In the future, it is crucial to focus on improving public awareness and education regarding herbicide safety. This involves addressing misconceptions and promoting informed decision-making regarding the impact of herbicides on food safety (Katre et al. 2022). Engaging consumers in a constructive dialogue about herbicide safety should be a priority to achieve this, and educational campaigns and outreach programs should be developed, targeting consumers, farmers, and stakeholders (Douthwaite and Hoffecker 2017; Katre et al. 2022). To ensure accurate and accessible information on herbicide safety reaches the public, collaboration between regulatory bodies, agricultural organizations, and public health agencies is essential. These entities should work together to effectively communicate the risks and benefits associated with herbicide use and this can be achieved through clear communication of safety guidelines, regulations, and best practices (Benyam et al. 2021). It is important to empower individuals to make informed choices about their food consumption. To facilitate this, user-friendly online platforms and mobile applications should be developed to provide herbicide safety information (Nitin et al. 2020; Umapathi et al. 2022). Additionally, educational materials such as fact sheets and guidelines for safe herbicide handling and application should be made widely available (Ndayambaje et al. 2019). Incorporating herbicide safety information into agricultural extension services and training programs can further enhance awareness among farmers and those involved in the agricultural industry (Ngowi et al. 2016; Berni et al. 2021).
Collaboration between the agricultural industry, research institutions, and public health agencies should be fostered to promote joint initiatives for research, education, and outreach activities focused on herbicide safety (Ervin and Frisvold 2016; Berni et al. 2021). Engaging community organizations and non-governmental organizations (NGOs) can also play a vital role in facilitating the dissemination of knowledge on herbicide safety (Wiedemann et al. 2022). Furthermore, conducting epidemiological studies to assess potential health effects of long-term herbicide exposure and longitudinal studies on the environmental persistence and impact of herbicide residues will contribute to a more comprehensive understanding of herbicide safety. Collaborative research efforts should be undertaken to evaluate the effectiveness of alternative weed management practices, reducing reliance on herbicides (Riemens et al. 2022). To ensure the integration of herbicide safety and sustainable agriculture education, it is important to incorporate these topics into school curricula. Encouraging student involvement in research projects and initiatives related to herbicide safety can foster innovation and a deeper understanding of the subject (Wiedemann et al. 2022). Eventually, supporting the development of educational resources and materials for young learners is crucial for building a solid foundation of knowledge on herbicide safety. By addressing these future challenges and focusing on research in these directions, can make significant progress in enhancing public awareness and education on herbicide safety.
Regulatory aspects associated with herbicide usage
Regulations associated with the herbicide usage encompass a complex web of policies and guidelines aimed at ensuring environmental safety, human health protection, and effective management of herbicidal products. Regulatory bodies worldwide often institute stringent measures governing the registration, sale, and application of herbicides, requiring thorough testing for toxicity, environmental impact, and efficacy before approval (Reeves et al. 2019; Valbuena et al. 2021). Additionally, herbicide labeling requirements detailing proper usage, safety precautions, and environmental risks are mandated to inform users adequately (Valbuena et al. 2021). Periodic reassessment and monitoring of herbicide residues in food, water, and soil are crucial for maintaining compliance with regulatory standards. Striking a balance between agricultural needs and environmental sustainability remains a continuous challenge in herbicide regulation.
Conclusions and future perspectives
The application of herbicides is crucial in modern agriculture worldwide. However, improper use of these chemicals can threaten human and environmental health. In fact, excessive and repeated use of herbicides over an extended period can lead to the development of resistance in weed species toward specific weedicides. Furthermore, the offsite migration of herbicides through runoff and leaching can contaminate surface and groundwater, thereby adversely affecting aquatic organisms. Recent trends indicate a shift towards more precise and targeted formulations of herbicides, increased utilization of systemic and pre-emergence herbicides, and decreased overall herbicide usage. However, global agriculture encounters numerous challenges due to the adverse environmental impacts stemming from herbicide contamination, both at application site and offsite. Due to growing concerns, it is crucial to innovate herbicides with better selectivity or develop bio-based alternatives. Enzyme inhibitors and receptor-based herbicides can offer precise weed control and reduce ecological implications. Rapidly-degrading herbicides or those binding firmly to soil particles are needed to prevent groundwater or surface water contamination. Sustainable weed management practices, like using remote sensing, drones, and machine learning, can enable real-time weed detection and targeted herbicide application. Public awareness and constructive dialogue about herbicide safety should be prioritized through educational campaigns targeting consumers, farmers, and stakeholders.
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Parven, A., Meftaul, I.M., Venkateswarlu, K. et al. Herbicides in modern sustainable agriculture: environmental fate, ecological implications, and human health concerns. Int. J. Environ. Sci. Technol. (2024). https://doi.org/10.1007/s13762-024-05818-y
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DOI: https://doi.org/10.1007/s13762-024-05818-y