Vincenzo Trotta
Oussama Baaloudj
Monica Brienza- 1School of Agricultural Forestry, Food and Environmental Sciences (SAFE), University of Basilicata, Potenza, Italy
- 2Department of Science, University of Basilicata, Potenza, Italy
Rapid urbanization has heightened the urgency of the necessity for sustainable water management in agriculture. This review focuses on the impacts of using reused wastewater in agricultural practices, specifically highlighting the nutrient benefits and consequences of pollutants on important environmental elements. It investigates the impact of contaminants on agricultural ecosystems by assessing the soil composition and nutrient equilibrium. This research also examines the impact of pollution exposure on plants and insects, elucidating the behavioural adaptations and their broader ecological consequences in agricultural environments. Eventually, a comprehensive analysis was conducted to consolidate these findings, emphasizing the challenges and significance of implementing sustainable practices. This study highlights the necessity of addressing the health and environmental concerns associated with the agricultural reuse of wastewater, while also giving valuable information to guide future regulations.
Introduction
Soil health and water scarcity affect various human activities, including agricultural irrigation, food and energy production, manufacturing, drinking water supply, and ecosystem preservation (Shahriar et al., 2021). It has been estimated that 20% of the Mediterranean population experiences chronic water stress, with over 50% of that number being impacted by water stress during the summer (EEA, 2021) and agriculture remains the activity that consumes 70% of fresh water (Meffe et al., 2021; Shannag et al., 2021). Globally, it has been estimated that over 20 million hectares of land are irrigated with non-conventional water resources (Rusănescu et al., 2022). The concept of using recycled wastewater for irrigation is not new; in fact, it dates back to about 3000 B.C., and although there are no precise global estimates of wastewater reuse, it is assumed that at least 7% of irrigated land uses wastewater (WHO, 2013). However, wastewater reuse in agriculture may be associated with environmental and human health risks due to the presence of salts, heavy metals, and organic contaminants that can lead to the contamination of soil, crops, and groundwater (Verma et al., 2023). Another negative effect associated with wastewater reuse is the potential spread of antibiotic-resistant bacteria, which can survive the inhibitory effects of common antibiotics (Bougnom and Piddock, 2017).
It is clear that the need to reuse unconventional water is leading the scientific community to improve its quality, and many research papers have been published on adsorption (Kamińska et al., 2022), photocatalysis (Foti et al., 2022), electrochemistry (Brienza and Garcia-Segura, 2022), etc. At the same time, research activities on wastewater reuse for agriculture started, but due to the fact that there is no clear regulation and it is often considered a forbidden practice in many countries, the research is developed at laboratory scale, greenhouse scale and really few at field scale. For this reason, the scientific literature on municipal wastewater treatment has grown exponentially over the past 10 years, and the amount of published research on agricultural water reuse has intensified, although the absolute number of publications on the latter argument is generally two orders of magnitude less than the former (Figure 1).
Figure 1. Distribution over time of publications extracted from Scopus (Elsevier) from 2013 to December 2023. Only publications containing the words “wastewater” AND “treatments” (A) and wastewater” AND “treatments” AND “agriculture” (B) in the title, abstract or keywords were included.
The chemical and physical properties of wastewater effluent are contingent upon its source and exhibit variations influenced by factors such as climate, socio-economic conditions, and the behavioural patterns of the local population (Gatta et al., 2021). Wastewater is a complex matrix of a wide variety of microorganisms, organic and inorganic compounds. Organic compounds range from carbohydrates, lignin, fats, proteins, household cleaning products, industrial products, pharmaceuticals, and personal care products. Inorganic substances include a variety of compounds, some of which have hazardous properties and contain heavy metals (Bawa, 2023). Microorganisms consist of various species, including pathogenic genera such as Trichuris, Ascaris, and Giardia (Zeleke et al., 2021).
The use of wastewater for irrigation has both advantages and disadvantages for agricultural applications. However, its main problem is that the addition of nutrients, any contaminants or residues in the wastewater can accumulate in the soil during irrigation and could be dangerous due to their uptake by crops (Margenat et al., 2019; Trotta et al., 2024). For this reason, proper risk assessment is required when considering the use of treated effluent for irrigation. The European Parliament and Council published the minimum requirements for agricultural irrigation (EUR-Lex, 2020). For examples, in food and root crops consumed raw where the edible part is in direct contact with reclaimed water, the number of E. coli/100 mL should be ≤10, BOD5 (mg/L) ≤ 10, TSS (mg/L) ≤ 10, turbidity (NTU) ≤ 5, Legionella spp.: <1,000 cfu/L, intestinal nematodes (helminth eggs): ≤1 egg/L. The presence of pollutants in wastewater makes it necessary to study their effects on soil, plants, pests, and human health, but at the same time to improve conventional wastewater treatment by adding low-cost tertiary treatment to improve the quality of the effluent.
This review aims to provide an overview of the benefits and environmental risks associated with the use of wastewater in agricultural irrigation and to assess the ecological consequences.
Harvesting opportunities: benefits of using wastewater in agriculture
The use of wastewater presents both challenges and opportunities. Its use can lead to positive outcomes for farmers, society, and municipalities, as its nutrient content can be effectively used in agricultural and other productive activities (Belhaj et al., 2016; Hettiarachchi et al., 2018). Wastewater has a substantial effect on crop production by enhancing yields (Ofori et al., 2021), improving soil performance, increasing soil microbial activity, and enhancing its physical structure (Zhang and Shen, 2019). From an economic perspective, this practice has the potential to reduce fertilizer use and freshwater consumption for irrigation, with benefits to the local economy (Avadí et al., 2022). The European Parliament and Council are reinforcing the use of wastewater to preserve water resources and promote a circular economy, protecting human health and ensuring the adequate collection, treatment, and discharge of urban and industrial waste waters (EUR-Lex, 2020). It is well known that wastewater sludge is a source of nutrients, but it can also be turned into biogas for profitable use (Elalami et al., 2019). Mavhungu et al. (2020) reported an interesting pilot-scale study in which it was demonstrated through a zero liquid discharge that 3.5 m3 of municipal wastewater it was possible to simultaneously recover struvite (52.5 kg) useful for the agricultural industry and 3.4 m3 of drinking water. In addition, wastewater can be a source of rare earth elements, as demonstrated by Al Momani et al. (2023).
The first environmental matrix to benefit from wastewater irrigation is the soil. In addition to its nutrient content to reduce fertilizer dosage in agricultural activities, wastewater is free from climate impacts, low-cost and could positively influence soil performance since contains dissolved organic matter, improves soil physical structure, and increases soil microbial activity (Dang et al., 2019). The levels of nutrients introduced by wastewater increase soil fertility and can be safe for short cultivation crops such as lettuce (Urbano et al., 2017) or eggplant and tomato (Cirelli et al., 2012). Lettuce irrigated with treated wastewater had higher leaf macronutrients (N, P, K, Ca, Mg, and S), higher fresh weight (+50% in the first cycle and +100% in the second), and greater root surface area than lettuce irrigated with drinking water (Urbano et al., 2017). In addition, tomato plants irrigated with treated municipal wastewater produced higher yields (about 20%) than plants irrigated with fresh water and increased the number of marketable fruits (Cirelli et al., 2012). Another relevant positive aspect of these studies was the safety of lettuce from the presence of Escherichia coli on the leaves or in the soil, and the high microbiological quality of eggplant and tomato. After the soil, plants are the first level of the trophic chain that includes herbivorous insects, predators, and pollinators, and the use of reclaimed wastewater for crop irrigation raises the attention to the interaction between plants and insect pests. Contaminated wastewater can negatively shape the population dynamics of insect pests in an agroecosystem by affecting plant growth and physiology through bottom-up effects involving uptake and translocation of contaminants or increased salinity stress (Dong et al., 2020; Ghodoum Parizipour et al., 2021). Wastewater irrigation can also increase the chemical defenses of plants, reducing their nutritional quality for herbivorous insects, and thus contributing positively to pest management programs (Güntner et al., 1997; Han et al., 2016). In addition, contaminated wastewater can adversely affect the fitness of pest insects through direct ingestion of chemicals accumulated in non-edible plant parts (Culliney et al., 1986).
Highlighting challenges: risks in wastewater use in agriculture
While water reuse offers many benefits, the scientific community has identified several human health and environmental concerns and challenges (Helmecke et al., 2020). The higher nutrient levels in wastewater may have positive effects on plant growth but also on herbivorous insect performance, and it is not obvious that the more vigorous plants are able to mitigate the negative consequence of higher pest infestation (Price, 1991; Shannag et al., 2021). Under this scenario, pesticide use would increase.
Urban wastewater treatment plants typically discharge effluents containing a wide range of organic chemicals, toxic metals, and microbial pathogens (Salgot et al., 2006). These effluents present a number of potential hazards related to the presence of contaminants in the soil. In this sense, there are considerable concerns about the potential risks to human wellbeing, including the contamination of potable water and the accumulation of harmful substances in consumable agricultural products (Shuval et al., 1997).
Another serious problem associated with the weakness of wastewater treatment systems is bacterial contamination. In fact, the presence of elevated levels of pathogens and microbial hazards also raises concerns about their impact on human welfare (Deb, 2018). The potential risks may result in adverse health effects, including (but not limited to) diarrhea and parasitic infections, microbial outbreaks, skin disorders, and systemic infections (Stec et al., 2022). Besides health consequences, nitrosamines are carcinogenic to multiple organs in at least 40 animal species (Bogovski and Bogovski, 1981). The ubiquitously occurrence of N- nitrosamine in different environmental compartments including surface and ground waters (Ma et al., 2012), sludge (Venkatesan et al., 2014), and soil (Chiron and Duwig, 2016) has been reported. Research on N-nitrosamines has been mainly limited to those compounds included in the US EPA Contaminant Candidate List 3, namely, N-nitroso-diethylamine (NDEA), NDMA, N-nitroso-di-n-propylamine (NDPA), N-nitroso-diphenylamine (NDPhA), N-nitroso-pyrrolidine (NPYR). However, all secondary and tertiary amines can theoretically undergo nitrosation reactions and there is no clear rationale for only targeting those particular compounds. So, it has demonstrated that these compounds can be generated during wastewater treatmen, as reported by Brienza et al. (2020), on the case of the fate of Ciprofloxacin under denitrification sludge treatment. In addition, these substances are among the most common chemical pollutants identified in groundwater aquifers worldwide (Zhang et al., 2020). The presence of phosphorus has a substantial influence on surface water, the reaction between nitrogen (N) and phosphorus (P) compounds in water presents significant hazards to both the environment and human health (Nieder et al., 2018). The absence of NO might have detrimental consequences since it can potentially cause the death of denitrification microorganisms (Brienza et al., 2017). The presence of these bacteria is essential to maintaining the overall health of the ecosystem, and their ability to survive is extremely important. In addition, the presence of N-nitroso compounds as impurities can potentially harm these microorganisms, exacerbating environmental problems (Ahamad et al., 2020). The presence of antibiotics in wastewater can also contribute to amplifying the risk of antibiotic resistance by exerting selective pressure, promoting gene transfer, and sustaining resistant bacterial populations (Guo and Kong, 2019).
Currently, there is little knowledge of the effects of antibiotics at environmental concentrations on terrestrial insects (both beneficial and pest) or their microbial community composition. For example, most common pharmaceutical (including antibiotics) and personal care products found in reclaimed water negatively affect the life history traits of the agricultural pest Trichoplusia ni (Lepidoptera: Noctuidae) thought an influence on its microbial communities (Pennington et al., 2017). Also, pharmaceuticals and personal care products at environmentally concentrations can negatively influence the development of Culex mosquitoes (Pennington et al., 2016). However, although the use of wastewater in integrated pest management programs seems promising (pesticide rates would be reduced or pests would become more susceptible), it is possible that these chemicals could be transferred to consumed crops, and we do not yet know their potential effects on human health.
The widespread presence of urban pest control insecticides, such as fipronil and imidacloprid, and their principal transformation products, has been consistently observed in wastewater analyses (Sadaria et al., 2017). In the context of ecological implications, it is noteworthy that insects, particularly pollinators, exhibit heightened sensitivity to these chemical agents compared to aquatic organisms. The utilization of wastewater contaminated with these insecticides for irrigation introduces a concerning dimension, as it may have discernible negative effects on the life history traits of insect pollinators. This concern is particularly relevant due to the potential for pollinators to experience chronic exposure to these pesticides through various routes throughout the foraging season (Krupke et al., 2012; Sadaria et al., 2017; Carter et al., 2020).
Strategies for safer and productive wastewater reuse in agriculture
Efforts to minimize the risks of agricultural wastewater reuse include the development of a comprehensive risk management strategy, the advancement of sophisticated methods to eliminate hazardous chemicals, and the adoption of guidelines to ensure the protection of human health during agricultural wastewater reuse (Al-Hazmi et al., 2023). The challenges that come with using wastewater for irrigation are well documented and include several dimensions, namely, economic, environmental, social, and health challenges (Singh et al., 2018). In many countries, extensive wastewater collection and treatment is seen as a long-term strategy for the future due to the scarcity of financial and technological resources (Bdour et al., 2009). To achieve this goal, it is also important to reduce chemical and biological oxygen demand, total suspended solids, and total bacteria counts (Iqbal et al., 2022). A multitude of conventional wastewater treatment facilities have employed a combination of physical, chemical, and biological processes to mitigate the concentrations of solids as well as diverse organic and inorganic compounds (Hai et al., 2007). A variety of techniques, such as adsorption, photocatalysis, electrochemistry, filtration, sedimentation, and flotation, are employed to efficiently eradicate both inorganic and organic particulate matter. In order to maximize the benefits derived from wastewater, it is insufficient to solely assess the associated risks. Careful consideration of the amount of crop nutrients added to the soil by wastewater in irrigation is essential.
The implementation of suitable irrigation systems in agriculture is also crucial for more sustainable wastewater reuse. Different irrigation methods, such as subsurface irrigation, drip irrigation, furrow irrigation, and sprinkler systems offer varying advantages (Eisenhauer et al., 2021). An example is drip irrigation, which delivers water directly to the root zone of plants, minimizing the interaction between wastewater and plant leaves, thereby reducing the risk of pathogen transfer and soil contamination (Ungureanu et al., 2020). In addition, the use of modern irrigation technology allows for better regulation of water application rates and timing, maximizing water use efficiency and minimizing the risk of excessive irrigation (Valipour and Singh, 2016).
Inoculation with endophytic plant growth-promoting fungi is also considered a valid strategy to mitigate the negative effects of stress caused by wastewater reuse in agriculture (OECD, 2023). These organisms are able to promote plant resistance and mitigate the effects of biotic and abiotic stresses by producing phytohormones and antioxidants (Studholme et al., 2013).
Discussion
As highlighted in the review, the benefits of wastewater reuse, including its nutrient composition and potential economic benefits, are very clear. However, it is important to promptly address the inherent hazards caused by contaminants and pathogens found in untreated or inadequately treated wastewater. The possibility of sustainable wastewater reuse in agriculture depends on the implementation of interdisciplinary approaches (Wichelns et al., 2015). Collaboration among environmental scientists, agronomists, engineers, public health experts, policymakers and other relevant stakeholders is essential. Interdisciplinary research initiatives have the potential to provide comprehensive and holistic perspectives on the complex dynamics associated with the reuse of wastewater. Such initiatives facilitate the formulation of comprehensive strategies that address multiple dimensions, including environmental, agricultural, and public health considerations (Santos et al., 2023). It is important to note that current wastewater treatment systems have certain limitations in their ability to completely remove specific emerging contaminants (Younas et al., 2021). It is important to develop treatment methods that are both innovative and advanced in their ability to effectively remove a wider range of contaminants, such as persistent organic pollutants and pathogens (Gaur et al., 2018; Guerra-Rodríguez et al., 2023). The incorporation of emerging technologies, such as nanotechnology, membrane filtration, and advanced oxidation processes, has the potential to significantly improve the overall quality of treated wastewater (Baaloudj et al., 2022). Implementing more sustainable practices in the use of wastewater is particularly important in arid and semi-arid regions, where the focus should be on building dedicated plants specifically designed for agricultural and landscape irrigation purposes (Rusănescu et al., 2022). Table 1 summarizes, based on the literature, various risks of reusing wastewater in agriculture, including their potential impacts and possible mitigation strategies.
Table 1. Risks of using wastewater in agriculture and current mitigation strategies.
Perspectives
The complexity of using wastewater for agricultural irrigation requires a comprehensive, multi-faceted strategy. Long-term studies to achieve sustainable food production are of great importance, especially when it comes to evaluating the rates at which carbon, nitrogen and phosphorus are converted (Powlson et al., 2011). Global monitoring of organic persistent emerging contaminants and pathogens in irrigated soils has the potential to provide effective strategies for pollution reduction. Understanding the environmental fate of emerging contaminants and identifying harmful by-products of wastewater in soils is essential for conducting a thorough risk assessment. In parallel, understanding the impact of biologically active, pseudopersistent pharmaceuticals in reclaimed water on agricultural ecosystems and the implications for integrated pest management practices must be a research priority. In addition, developing cost-effective wastewater treatment systems and improving water quality at the source are critical to promoting sustainable wastewater reuse in agricultural practices, thereby protecting environmental integrity and human health (Obaideen et al., 2022). It is appropriate to use innovative and advanced tertiary wastewater treatment based on disinfection and decontamination in accordance with the guidelines of the Clean Water Act or of the Water Framework Directive of the European Parliament and Council, which aims to combat water pollution.
Author contributions
VT: Writing–original draft, Writing–review and editing. OB: Writing–original draft. MB: Conceptualization, Funding acquisition, Writing–review and editing.
Funding
The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This research received funding from MUR under the umbrella of the PRIMA-Partnership for Research and Innovation in the Mediterranean Area through the research project SAFE ID project 1826 “Sustainable water reuse practices improving safety in agriculture, food and environment”.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Ahamad, A., Madhav, S., Singh, A. K., Kumar, A., and Singh, P. (2020). “Types of water pollutants: conventional and emerging BT - sensors in water pollutants monitoring: role of material,” eds. D. Pooja, P. Kumar, P. Singh, and S. Patil (Singapore: Springer Singapore), 21–41. doi:10.1007/978-981-15-0671-0_3
Al-Hazmi, H. E., Mohammadi, A., Hejna, A., Majtacz, J., Esmaeili, A., Habibzadeh, S., et al. (2023). Wastewater reuse in agriculture: prospects and challenges. Environ. Res. 236, 116711. doi:10.1016/j.envres.2023.116711
Al Momani, D. E., Al Ansari, Z., Ouda, M., Abujayyab, M., Kareem, M., Agbaje, T., et al. (2023). Occurrence, treatment, and potential recovery of rare earth elements from wastewater in the context of a circular economy. J. Water Process Eng. 55, 104223. doi:10.1016/j.jwpe.2023.104223
Aslam, A., Naz, A., Shah, S. S. H., Rasheed, F., Naz, R., Kalsom, A., et al. (2023). Heavy metals contamination in vegetables irrigated with wastewater: a case study of underdeveloping regions of Pakistan. Environ. Geochem Health 45, 8911–8927. doi:10.1007/s10653-023-01662-0
Avadí, A., Benoit, P., Bravin, M. N., Cournoyer, B., Feder, F., Galia, W., et al. (2022). in Chapter Two - trace contaminants in the environmental assessment of organic waste recycling in agriculture: gaps between methods and knowledge. Editor A. Sparks (Academic Press), 53–188. doi:10.1016/bs.agron.2022.03.002
Baaloudj, O., Nasrallah, N., Bouallouche, R., Kenfoud, H., Khezami, L., and Assadi, A. A. (2022). High efficient Cefixime removal from water by the sillenite Bi12TiO20: photocatalytic mechanism and degradation pathway. J. Clean. Prod. 330, 129934. doi:10.1016/j.jclepro.2021.129934
Bawa, U. (2023). Heavy metals concentration in food crops irrigated with pesticides and their associated human health risks in Paki, Kaduna State, Nigeria. Cogent Food Agric. 9. doi:10.1080/23311932.2023.2191889
Bdour, A. N., Hamdi, M. R., and Tarawneh, Z. (2009). Perspectives on sustainable wastewater treatment technologies and reuse options in the urban areas of the Mediterranean region. Desalination 237, 162–174. doi:10.1016/j.desal.2007.12.030
Belhaj, D., Jerbi, B., Medhioub, M., Zhou, J., Kallel, M., and Ayadi, H. (2016). Impact of treated urban wastewater for reuse in agriculture on crop response and soil ecotoxicity. Environ. Sci. Pollut. Res. 23, 15877–15887. doi:10.1007/s11356-015-5672-3
Bogovski, P., and Bogovski, S. (1981). Special report animal species in which n-nitroso compounds induce cancer. Int. J. Cancer 27, 471–474. doi:10.1002/ijc.2910270408
Bougnom, B. P., and Piddock, L. J. V. (2017). Wastewater for urban agriculture: a significant factor in dissemination of antibiotic resistance. Environ. Sci. Technol. 51, 5863–5864. doi:10.1021/acs.est.7b01852
Brienza, M., Duwig, C., Pérez, S., and Chiron, S. (2017). 4-nitroso-sulfamethoxazole generation in soil under denitrifying conditions: field observations versus laboratory results. J. Hazard Mater 334, 185–192. doi:10.1016/j.jhazmat.2017.04.015
Brienza, M., and Garcia-Segura, S. (2022). Electrochemical oxidation of fipronil pesticide is effective under environmental relevant concentrations. Chemosphere 307, 135974. doi:10.1016/j.chemosphere.2022.135974
Brienza, M., Manasfi, R., Sauvêtre, A., and Chiron, S. (2020). Nitric oxide reactivity accounts for N-nitroso-ciprofloxacin formation under nitrate-reducing conditions. Water Res. 185, 116293. doi:10.1016/j.watres.2020.116293
Carter, L. J., Agatz, A., Kumar, A., and Williams, M. (2020). Translocation of pharmaceuticals from wastewater into beehives. Environ. Int. 134, 105248. doi:10.1016/j.envint.2019.105248
Chen, W., Lu, S., Pan, N., and Jiao, W. (2013). Impacts of long-term reclaimed water irrigation on soil salinity accumulation in urban green land in Beijing. Water Resour. Res. 49, 7401–7410. doi:10.1002/wrcr.20550
Cheng, M., Wang, H., Fan, J., Wang, X., Sun, X., Yang, L., et al. (2021). Crop yield and water productivity under salty water irrigation: a global meta-analysis. Agric. Water Manag. 256, 107105. doi:10.1016/j.agwat.2021.107105
Chiron, S., and Duwig, C. (2016). Biotic nitrosation of diclofenac in a soil aquifer system (Katari watershed, Bolivia). Sci. Total Environ. 565, 473–480. doi:10.1016/j.scitotenv.2016.05.048
Cirelli, G. L., Consoli, S., Licciardello, F., Aiello, R., Giuffrida, F., and Leonardi, C. (2012). Treated municipal wastewater reuse in vegetable production. Agric. Water Manag. 104, 163–170. doi:10.1016/j.agwat.2011.12.011
Collivignarelli, M. C., Abbà, A., Alloisio, G., Gozio, E., and Benigna, I. (2017). Disinfection in wastewater treatment plants: evaluation of effectiveness and acute toxicity effects. Sustainability 9, 1704. doi:10.3390/su9101704
Culliney, T. W., Pimentel, D., and Lisk, D. J. (1986). Impact of chemically contaminated sewage sludge on the collard arthropod community. Environ. Entomol. 15, 826–833. doi:10.1093/ee/15.4.826
Dang, Q., Tan, W., Zhao, X., Li, D., Li, Y., Yang, T., et al. (2019). Linking the response of soil microbial community structure in soils to long-term wastewater irrigation and soil depth. Sci. Total Environ. 688, 26–36. doi:10.1016/j.scitotenv.2019.06.138
Deb, P. (2018). “Chapter 14 - environmental pollution and the burden of food-borne diseases,” in Handbook of food bioengineering. Editors A. M. Holban, and A. M. B. T.-F. D. Grumezescu (Academic Press), 473–500. doi:10.1016/B978-0-12-811444-5.00014-2
Dong, Y. C., Wang, Z. J., Bu, R. Y., Dai, H. J., Zhou, L. J., Han, P., et al. (2020). Water and salt stresses do not trigger bottom-up effects on plant-mediated indirect interactions between a leaf chewer and a sap-feeder. J. Pest Sci. 93, 1267–1280. (2004. doi:10.1007/s10340-020-01258-y
EEA (2021). World water day: turning to nature for solutions. Copenhagen, Denamerk: Environmental European Agency. Available at: https://www.eea.europa.eu/highlights/world-water-day-turning-to (Accessed October 12, 2023).
Eisenhauer, D. E., Martin, D. L., Heeren, D. M., and Hoffman, G. J.American Society of Agricultural and Biological Engineers (2021). Irrigation systems management. St. Joseph, MI. USA: American Society of Agricultural and Biological Engineers, 49085–49659. (ASABE).
Elalami, D., Carrere, H., Monlau, F., Abdelouahdi, K., Oukarroum, A., and Barakat, A. (2019). Pretreatment and co-digestion of wastewater sludge for biogas production: recent research advances and trends. Renew. Sustain. Energy Rev. 114, 109287. doi:10.1016/j.rser.2019.109287
EUR-Lex (2020). Regulation (EU) 2020/741 of the European Parliament and of the Council of 25 May 2020 on minimum requirements for water reuse (Text with EEA relevance). Available at: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32020R0741 (Accessed January 10, 2024).
Foti, L., Coviello, D., Zuorro, A., Lelario, F., Bufo, S. A., Scrano, L., et al. (2022). Comparison of sunlight-AOPs for levofloxacin removal: kinetics, transformation products, and toxicity assay on Escherichia coli and Micrococcus flavus. Environ. Sci. Pollut. Res. 29, 58201–58211. doi:10.1007/s11356-022-19768-w
Friedler, E., Kovalio, R., and Ben-Zvi, A. (2006). Comparative study of the microbial quality of greywater treated by three on-site treatment systems. Environ. Technol. 27, 653–663. doi:10.1080/09593332708618674
Gatta, G., Libutti, A., Gagliardi, A., Disciglio, G., Tarantino, E., Beneduce, L., et al. (2021). “Wastewater reuse in agriculture: effects on soil-plant system properties BT - interaction and fate of pharmaceuticals in soil-crop systems: the impact of reclaimed wastewater,” eds. S. Pérez Solsona, N. Montemurro, S. Chiron, and D. Barceló (Cham: Springer International Publishing), 79–102. doi:10.1007/698_2020_648
Gaur, N., Narasimhulu, K., and PydiSetty, Y. (2018). Recent advances in the bio-remediation of persistent organic pollutants and its effect on environment. J. Clean. Prod. 198, 1602–1631. doi:10.1016/j.jclepro.2018.07.076
Ghodoum Parizipour, M. H., Rajabpour, A., Jafari, S., and Tahmasebi, A. (2021). Host-targeted salt stress affects fitness and vector performance of bird cherry-oat aphid (Rhopalosiphum padi L.) on wheat. Arthropod Plant Interact. 15, 47–58. doi:10.1007/s11829-020-09795-0
Guerra-Rodríguez, S., Abeledo-Lameiro, M. J., Polo-López, M. I., Plaza-Bolaños, P., Agüera, A., Rodríguez, E., et al. (2023). Pilot-scale sulfate radical-based advanced oxidation for wastewater reuse: simultaneous disinfection, removal of contaminants of emerging concern, and antibiotic resistance genes. Chem. Eng. J. 477, 146916. doi:10.1016/j.cej.2023.146916
Güntner, C., Vázquez, Á., González, G., Usubillaga, A., Ferreira, F., Moyna, P., et al. (1997). Effect of Solanum glycoalkaloids on potato aphid, Macrosiphum euphorbiae. J. Chem. Ecol. 23, 1651–1659. doi:10.1023/b:joec.0000006429.14373.91
Guo, M.-T., and Kong, C. (2019). Antibiotic resistant bacteria survived from UV disinfection: safety concerns on genes dissemination. Chemosphere 224, 827–832. doi:10.1016/j.chemosphere.2019.03.004
Hai, F. I., Yamamoto, K., and Fukushi, K. (2007). Hybrid treatment systems for dye wastewater. Crit. Rev. Environ. Sci. Technol. 37, 315–377. doi:10.1080/10643380601174723
Han, P., Desneux, N., Michel, T., Le Bot, J., Seassau, A., Wajnberg, E., et al. (2016). Does plant cultivar difference modify the bottom-up effects of resource limitation on plant-insect herbivore interactions? J. Chem. Ecol. 42, 1293–1303. doi:10.1007/s10886-016-0795-7
Helmecke, M., Fries, E., and Schulte, C. (2020). Regulating water reuse for agricultural irrigation: risks related to organic micro-contaminants. Environ. Sci. Eur. 32, 4. doi:10.1186/s12302-019-0283-0
Hettiarachchi, H., Caucci, S., and Ardakanian, R. (2018). “Safe use of wastewater in agriculture: the golden example of nexus approach BT - safe use of wastewater in agriculture: from concept to implementation,” eds. H. Hettiarachchi, and R. Ardakanian (Cham: Springer International Publishing), 1–11. doi:10.1007/978-3-319-74268-7_1
Iqbal, M., Nauman, S., Ghafari, M., Parnianifard, A., Gomes, A., and Gomes, C. (2022). Treatment of wastewater for agricultural applications in regions of water scarcity. Biointerface Res. Appl. Chem. 12, 6336–6360. doi:10.33263/BRIAC125.63366360
Jacquet, F., Jeuffroy, M. H., Jouan, J., Le Cadre, E., Litrico, I., Malausa, T., et al. (2022). Pesticide-free agriculture as a new paradigm for research. Agron. Sustain Dev. 42, 8–24. doi:10.1007/s13593-021-00742-8
Kamińska, G., Marszałek, A., Kudlek, E., Adamczak, M., and Puszczało, E. (2022). Innovative treatment of wastewater containing of triclosan – SBR followed by ultrafiltration/adsorption/advanced oxidation processes. J. Water Process Eng. 50, 103282. doi:10.1016/j.jwpe.2022.103282
Keraita, B., Konradsen, F., Drechsel, P., and Abaidoo, R. C. (2007). Reducing microbial contamination on wastewater-irrigated lettuce by cessation of irrigation before harvesting. Trop. Med. Int. Health 12, 8–14. doi:10.1111/j.1365-3156.2007.01936.x
Khan, M. N., Aslam, M. A., Muhsinah, A. B., and Uddin, J. (2023). Heavy metals in vegetables: screening health risks of irrigation with wastewater in peri-urban areas of bhakkar, Pakistan. Toxics 11, 460. doi:10.3390/toxics11050460
Khan, S., Cao, Q., Zheng, Y. M., Huang, Y. Z., and Zhu, Y. G. (2008). Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ. Pollut. 152, 686–692. doi:10.1016/j.envpol.2007.06.056
Krupke, C. H., Hunt, G. J., Eitzer, B. D., Andino, G., and Given, K. (2012). Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One 7, e29268. doi:10.1371/journal.pone.0029268
Liu, C., Wang, J., Huang, P., Hu, C., Gao, F., Liu, Y., et al. (2023). Response of soil microenvironment and crop growth to cyclic irrigation using reclaimed water and brackish water. Plants 12, 2285. doi:10.3390/plants12122285
Ma, F., Wan, Y., Yuan, G., Meng, L., Dong, Z., and Hu, J. (2012). Occurrence and source of nitrosamines and secondary amines in groundwater and its adjacent jialu river basin, China. Environ. Sci. Technol. 46, 3236–3243. doi:10.1021/es204520b
Margenat, A., Matamoros, V., Díez, S., Cañameras, N., Comas, J., and Bayona, J. M. (2019). Occurrence and human health implications of chemical contaminants in vegetables grown in peri-urban agriculture. Environ. Int. 124, 49–57. doi:10.1016/j.envint.2018.12.013
Mavhungu, A., Masindi, V., Foteinis, S., Mbaya, R., Tekere, M., Kortidis, I., et al. (2020). Advocating circular economy in wastewater treatment: struvite formation and drinking water reclamation from real municipal effluents. J. Environ. Chem. Eng. 8, 103957. doi:10.1016/j.jece.2020.103957
Meffe, R., de Santiago-Martín, A., Teijón, G., Martínez Hernández, V., López-Heras, I., Nozal, L., et al. (2021). Pharmaceutical and transformation products during unplanned water reuse: insights into natural attenuation, plant uptake and human health impact under field conditions. Environ. Int. 157, 106835. doi:10.1016/j.envint.2021.106835
Nieder, R., Benbi, D. K., and Reichl, F. X. (2018). “Reactive water-soluble forms of nitrogen and phosphorus and their impacts on environment and human health BT - soil components and human health,” in , eds. R. Nieder, D. K. Benbi, and F. X. Reichl (Dordrecht: Springer Netherlands), 223–255. doi:10.1007/978-94-024-1222-2_5
Obaideen, K., Shehata, N., Sayed, E. T., Abdelkareem, M. A., Mahmoud, M. S., and Olabi, A. G. (2022). The role of wastewater treatment in achieving sustainable development goals (SDGs) and sustainability guideline. Energy Nexus 7, 100112. doi:10.1016/j.nexus.2022.100112
OECD (2023). OECD report on Water and agriculture: managing water sustainably is key to the future of food and agriculture. Available at: https://www.oecd.org/agriculture/topics/water-and-agriculture/(Accessed December 13, 2023).
Ofori, S., Puškáčová, A., Růžičková, I., and Wanner, J. (2021). Treated wastewater reuse for irrigation: pros and cons. Sci. Total Environ. 760, 144026. doi:10.1016/j.scitotenv.2020.144026
Othman, Y. A., Al-Assaf, A., Tadros, M. J., and Albalawneh, A. (2021). Heavy metals and microbes accumulation in soil and food crops irrigated with wastewater and the potential human health risk: a metadata analysis. Water (Basel) 13, 3405. doi:10.3390/w13233405
Pennington, M. J., Prager, S. M., Walton, W. E., and Trumble, J. T. (2016). Culex quinquefasciatus larval microbiomes vary with instar and exposure to common wastewater contaminants. Sci. Rep. 6, 21969–9. doi:10.1038/srep21969
Pennington, M. J., Rothman, J. A., Dudley, S. L., Jones, M. B., McFrederick, Q. S., Gan, J., et al. (2017). Contaminants of emerging concern affect Trichoplusia ni growth and development on artificial diets and a key host plant. Proc. Natl. Acad. Sci. 114, E9923-E9931–E9931. doi:10.1073/pnas.1713385114
Powlson, D. S., Gregory, P. J., Whalley, W. R., Quinton, J. N., Hopkins, D. W., Whitmore, A. P., et al. (2011). Soil management in relation to sustainable agriculture and ecosystem services. Food Policy 36, S72–S87. doi:10.1016/j.foodpol.2010.11.025
Price, P. W. (1991). The plant vigor hypothesis and herbivore attack. Oikos 62, 244–251. doi:10.2307/3545270
Rusănescu, C. O., Rusănescu, M., and Constantin, G. A. (2022). Wastewater management in agriculture. WaterSwitzerl. 14, 3351. doi:10.3390/w14213351
Sadaria, A. M., Sutton, R., Moran, K. D., Teerlink, J., Brown, J. V., and Halden, R. U. (2017). Passage of fiproles and imidacloprid from urban pest control uses through wastewater treatment plants in northern California, USA. Environ. Toxicol. Chem. 36, 1473–1482. doi:10.1002/etc.3673
Salgot, M., Huertas, E., Weber, S., Dott, W., and Hollender, J. (2006). Wastewater reuse and risk: definition of key objectives. Desalination 187, 29–40. doi:10.1016/j.desal.2005.04.065
Santos, E., Carvalho, M., and Martins, S. (2023). Sustainable water management: understanding the socioeconomic and cultural dimensions. Sustain. Switz. 15, 13074. doi:10.3390/su151713074
Santos, F., Almeida, C. M. R., Ribeiro, I., and Mucha, A. P. (2019). Potential of constructed wetland for the removal of antibiotics and antibiotic resistant bacteria from livestock wastewater. Ecol. Eng. 129, 45–53. doi:10.1016/j.ecoleng.2019.01.007
Shahriar, A., Tan, J., Sharma, P., Hanigan, D., Verburg, P., Pagilla, K., et al. (2021). Modeling the fate and human health impacts of pharmaceuticals and personal care products in reclaimed wastewater irrigation for agriculture. Environ. Pollut. 276, 116532. doi:10.1016/j.envpol.2021.116532
Shakir, E., Zahraw, Z., and Al-Obaidy, A. H. M. J. (2017). Environmental and health risks associated with reuse of wastewater for irrigation. Egypt. J. Petroleum 26, 95–102. doi:10.1016/j.ejpe.2016.01.003
Shannag, H. K., Al-Mefleh, N. K., and Freihat, N. M. (2021). Reuse of wastewaters in irrigation of broad bean and their effect on plant-aphid interaction. Agric. Water Manag. 257, 107156. doi:10.1016/j.agwat.2021.107156
Shuval, H., Lampert, Y., and Fattal, B. (1997). Development of a risk assessment approach for evaluating wastewater reuse standards for agriculture. Water Sci. Technol. 35, 15–20. doi:10.2166/wst.1997.0703
Singh, S., Ghosh, N. C., Gurjar, S., Krishan, G., Kumar, S., and Berwal, P. (2018). Index-based assessment of suitability of water quality for irrigation purpose under Indian conditions. Environ. Monit. Assess. 190, 29. doi:10.1007/s10661-017-6407-3
Stec, J., Kosikowska, U., Mendrycka, M., Stępień-Pyśniak, D., Niedźwiedzka-Rystwej, P., Bębnowska, D., et al. (2022). Opportunistic pathogens of recreational waters with emphasis on antimicrobial resistance—a possible subject of human health concern. Int. J. Environ. Res. Public Health 19, 7308. doi:10.3390/ijerph19127308
Studholme, D. J., Harris, B., Le Cocq, K., Winsbury, R., Perera, V., Ryder, L., et al. (2013). Investigating the beneficial traits of Trichoderma hamatum GD12 for sustainable agriculture-insights from genomics. Front. Plant Sci. 4, 258–313. doi:10.3389/fpls.2013.00258
Trotta, V., Russo, D., Rivelli, A. R., Battaglia, D., Bufo, S. A., Caccavo, V., et al. (2024). Wastewater irrigation and Trichoderma colonization in tomato plants: effects on plant traits, antioxidant activity, and performance of the insect pest Macrosiphum euphorbiae. Environ. Sci. Pollut. Res. 31, 18887–18899. doi:10.1007/s11356-024-32407-w
Ungureanu, N., Vlăduț, V., and Voicu, G. (2020). Water scarcity and wastewater reuse in crop irrigation. Sustainability 12, 9055. doi:10.3390/su12219055
Urbano, V. R., Mendonça, T. G., Bastos, R. G., and Souza, C. F. (2017). Effects of treated wastewater irrigation on soil properties and lettuce yield. Agric. Water Manag. 181, 108–115. doi:10.1016/j.agwat.2016.12.001
Valipour, M., and Singh, V. P. (2016). “Global experiences on wastewater irrigation: challenges and prospects,” in Balanced urban development: options and strategies for liveable cities. Editors B. Maheshwari, V. P. Singh, and B. Thoradeniya (Australia: Springer International Publishing), 289–327.
Venkatesan, A. K., Pycke, B. F. G., and Halden, R. U. (2014). Detection and occurrence of N-nitrosamines in archived biosolids from the targeted national sewage sludge survey of the U.S. Environmental protection agency. Environ. Sci. Technol. 48, 5085–5092. doi:10.1021/es5001352
Verma, K., Manisha, M., Shivali, N. U., Santrupt, R. M., Anirudha, T. P., Ramesh, N., et al. (2023). Investigating the effects of irrigation with indirectly recharged groundwater using recycled water on soil and crops in semi-arid areas. Environ. Pollut. 337, 122516. doi:10.1016/j.envpol.2023.122516
WHO (2013). Guidelines for the safe use of wastewater, excreta and greywater - volume 2. Ginevra éè, Switzerland: World Health Organization, United Nations Environment Programme, 222. Available at: https://www.who.int/publications/i/item/9241546832 (Accessed December 16, 2023).
Wichelns, D., Drechsel, P., and Qadir, M. (2015). “Wastewater: economic asset in an urbanizing world BT - wastewater: economic asset in an urbanizing world,”, eds. P. Drechsel, M. Qadir, and D. Wichelns (Dordrecht: Springer Netherlands), 3–14. doi:10.1007/978-94-017-9545-6_1
Younas, F., Mustafa, A., Farooqi, Z. U. R., Wang, X., Younas, S., Mohy-Ud-din, W., et al. (2021). Current and emerging adsorbent technologies for wastewater treatment: trends, limitations, and environmental implications. WaterSwitzerl. 13, 215. doi:10.3390/w13020215
Zeleke, A. J., Derso, A., Bayih, A. G., Gilleard, J. S., and Eshetu, T. (2021). Prevalence, infection intensity and associated factors of soil-transmitted helminthiasis among school-aged children from selected districts in northwest Ethiopia. Res. Rep. Trop. Med. 12, 15–23. doi:10.2147/RRTM.S289895
Zhang, M., Huang, G., Liu, C., Zhang, Y., Chen, Z., and Wang, J. (2020). Distributions and origins of nitrate, nitrite, and ammonium in various aquifers in an urbanized coastal area, south China. J. Hydrol. (Amst) 582, 124528. doi:10.1016/j.jhydrol.2019.124528
Keywords: wastewater reuse, contaminants, environmental risks, ecological consequences, sustainable agriculture
Citation: Trotta V, Baaloudj O and Brienza M (2024) Risks associated with wastewater reuse in agriculture: investigating the effects of contaminants in soil, plants, and insects. Front. Environ. Sci. 12:1358842. doi: 10.3389/fenvs.2024.1358842
Received: 20 December 2023; Accepted: 11 April 2024;
Published: 02 May 2024.
Edited by:
Arindam Malakar, University of Nebraska-Lincoln, United StatesReviewed by:
Cristina Couto, Cooperativa de Ensino Superior Politécnico e Universitário, PortugalHelder Gomes, Polytechnic Institute of Bragança (IPB), Portugal
Marzhan Kalmakhanova, M. Kh Dulati Taraz State University, Kazakhstan
Copyright © 2024 Trotta, Baaloudj and Brienza. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Monica Brienza, monica.brienza@unibas.it