A review of plant-based coagulants for turbidity and cyanobacteria blooms removal

In recent years, the proliferation of Harmful Cyanobacterial Blooms (CyanoHABs) has increased with water eutrophication and climate change, impairing human health and the environment in relation to water supply. In drinking water treatment plants (DWTPs), the bio-coagulation based on natural coagulants has been studied as an eco-friendly alternative technology to conventional coagulants for both turbidity and CyanoHABs removal. Plant-based coagulants have demonstrated their coagulation efficiency in turbidity removal, as reported in several papers but its ability in cyanobacterial removal is still limited. This paper mainly reviewed the application of plant-based coagulants in DWTPs, with focus on turbidity removal, including cyanobacterial cells. The future potential uses of these green coagulants to reduce noxious effects of cyanobacterial proliferation are presented. Green coagulants advantages and limitations in DWTPs are reviewed and discussed summarizing more than 10 years of knowledge.


Introduction
Harmful Cyanobacterial Blooms (CyanoHABs) in water supply systems become a worrying problem for water utilities worldwide (Anderson et al. 2002;Lopez et al., 2008). The frequency of occurrence of cyanobacteria blooms is Responsible Editor: Vitor VasconcelosVitor Vasconcelos 1 3 mainly related to the increase in nutrient inputs produced by the anthropogenic activities and global warming (Chapra et al., 2017;Heisler et al., 2008;O'Neil et al., 2012;Paerl et al., 2011;Paerl and Huisman, 2009;Rigosi et al., 2015). Moreover, the combination of several environmental factors such as water temperature, thermic stratification, salinity, light intensity, stagnation and residence time, and nutrients concentration increase can promote cyanobacteria proliferation (Merel et al., 2013).
Several treatment methods including conventional processes (Zamyadi et al., 2013) and more recently, the utilization of ultrasonic irradiation, ultra-violet (UV) irradiation, hydrodynamic cavitation, electrocoagulation-flotation processes and chemical oxidants such as chlorine, potassium permanganate and ozone (Qi et al., 2021) are used in DWTPs to sanitize water from cyanobacteria and their deleterious effects (Meglič et al., 2017). However, cyanobacteria cells and cyanotoxins, which can cause cyanobacteria cells to grow in sand filters and enter the successive treatment systems or even the distribution network (Joh et al., 2011;Shekhar et al., 2017), are not easily removed by all water treatment technologies (Tang et al., 2017). Moreover, the application of these strategies can be constrained by the high investments required.
Coagulation/flocculation (C/F) based on the addition of chemical coagulants and flocculants, such as aluminium salts and ferric chloride (Betatache et al., 2014;Chen et al., 2013), which promotes the agglomeration of particles, known as flocs (Ghosh et al., 1994;Shin et al., 2008). It is considered the most important process for the removal of cyanobacterial cells in conventional DWTPs. It has been reported up to 90% of intracellular cyanotoxins removal Sillanpää et al., 2018;Xagoraraki, 2007). Despite their efficiency in reducing turbidity and cyanobacterial cells, chemical coagulants and flocculants are still presenting detrimental effects, such as environmental pollution due to improper disposal of sludge, human health effects linked with the presence of residual alum in treated waters (Saleem and Bachmann, 2019;Simate et al., 2012), costly practices of sludge disposal and impacts on health and environment (Abdullah et al., 2016).
The aim of this review paper is to summarize and discuss: i) plant-based coagulants and their use in water supplies turbidity treatment, evidencing ii) the missing information to research on to harness their potential to address the problem of CyanoHABs as an alternative to conventional coagulants and flocculants, as well as iii) the applicability and future challenges in DWTPs.

Plant-based coagulants highlights
Recently, plant-based coagulants processes have become a major challenge for several scientists because of their efficiency, environmentally friendly behaviour compared to conventional coagulants, potential abundance and low cost (Antov et al., 2012;Betatache et al., 2014;Choy et al., 2016;Gautam et al., 2014;Šćiban et al., 2009).
Plant-based coagulants are made of polysaccharides or natural polymers, which are biodegradable, safe, easily available and easily accessible from reproducible agricultural resources (Asrafuzzaman et al., 2011;Bolto and Gregory, 2007;Bratby, 2006;Swati and Govindan, 2005). For instance, crude plant extracts are often available locally and can therefore be an inexpensive alternative to conventional coagulants. Moringa oleifera seeds is among the typical natural plant-based coagulants that is widely studied due to its efficiency performance to treat turbid water (Vunain et al., 2019). The plants such as rice starch and M. oleifera can be grown locally (Rasool et al., 2016;Ribau Teixeira et al., 2017). These reflections of producing coagulants could also strengthen societal aspect local populations depending on agricultural economics (Mahiya et al., 2016;Pondja Jr et al., 2017;Yin, 2010), guaranteeing the continuous supply of raw materials in the development of green coagulants (Mohd-Salleh et al., 2019).
Plant-based coagulants could also be obtained from agricultural wastes that are generally considered as not economically valuable having marketing constraints (Bories et al., 2009). Sutherland et al. (1994) stated that Moringa seeds are not only an oil source (40% wet weight of oil content), but after oil extraction, they can be reused as coagulants. Similarly, the derivatives from cassava (Manihot spp.) processing contain active coagulant agents (Heuzé et al., 2016;Howeler, 2001), based on natural polymers composed of proteins and polysaccharides (Mohd-Asharuddin et al., 2017;Zayadi et al., 2016). Several species from the Fabaceae family showed to contain chemicals that can be economically harvested to produce coagulants (Doyle 1994).
Plant-based coagulants are non-corrosive (Swati and Govindan, 2005) eliminating the risk of pipe erosions, and potentially carbon-neutral during their production process (Choy et al., 2014;Saleem and Bachmann, 2019). Moreover, they do not consume alkalinity, unlike chemical coagulants, and pH adjustments can be omitted (Choy et al., 2014). Operating costs in the water treatment sector are a great concern and plant-based coagulants seem an promising option (Kurita, 2006). Currently, Moringa cultivation costs approximately 2 USD /1 kg (i.e., ~ 3400 seeds), while 1 USD/1 kg is the alum salts quotation. Several efforts are necessary to really understand the life cycle impact analysis of these products and the role of the relative potential economy of scale, with particular reference to the social implications in local rural communities (Çoruh, 2005). Few data are available about the cost of raw coagulants as summarized in Table 1 where traditional and natural coagulants are compared (Çoruh, 2005). Bixler and Porse (2011) reported the unit price of some natural raw materials that reached the commercialization stage compared to chemical coagulants ( Table 1), suggesting that chemical materials can be more expensive than some natural raw materials. Even if some chemical coagulants can be less expensive, several factors can contribute to increase the management cost like the necessity to adjust the water pH. For example, alginate is more expensive than alum salts, but it is used in smaller amounts making it cheaper than alum salts (Bixler and Porse, 2011;Çorhu, 2005). (Çorhu, 2005) evidenced that cost values are calculated considering only the chemical costs and not the operational costs associated with further treatment of sludge from the coagulation/flocculation process, that could further increase the whole cost associated to the use of traditional coagulants. For example, it has been reported that alum sludge disposal requires ~ 130 USD/ton (Maidon et al., 2015). (Ndabigengesere and Subba Narasiah, 1998) showed that under the same dosing conditions (1 mL/L) M. oleifera seeds generated a sludge volume 1.2 10 -6 0.02 10 -6 1 10 -4 1 × 10 -7 -Initial turbidity in water (NTU) 5-100 80 -Raw material used as coagulant on the commercialization scale Unit price (USD/kg) 0.3-0.5* -1 12 19 Amount used (mg/L) 3 -80 0.2 -of 1.5 mL/L compared to the 7.5 mL/L produced by alum salts. Plant-based coagulants can generate an amount of sludge that is approximately five times lower than chemical coagulants  presenting suitable characteristics for agriculture reuse (Choy et al., 2014), with any further secondary pollution (Asrafuzzaman et al., 2011;Bolto and Gregory, 2007;Bratby, 2006;Swati and Govindan, 2005). The produced sludge is biodegradable and can be effectively degraded via biological methods (Renault et al., 2009). They can be disposed safely as soil fertilizer being not toxic (Gutierrez et al., 1998;Kaggwa et al., 2001;Mortula et al., 2009;Muisa et al., 2011;Verma et al., 2012b) thus reducing the cost of sludge management (Choy et al., 2014).

Potentialities of plant-based coagulants to remove turbidity from water
The effectiveness of plant-based coagulants was investigated by several authors to treat water contaminated by toxic cyanobacteria, excess of turbidity, heavy metals (Mahiya et al., 2016), including wastewater as well (Yin, 2010;Choy et al., 2015;Oladoja and Pan, 2015;Villaseñor-Basulto et al., 2018;Mohd-Salleh et al., 2019;Saleem and Bachmann, 2019). The application of plant-based coagulants for turbidity removal is summarized in Table 2 considering water test sample of water, type of extraction, contact time, initial turbidity and removal efficiency, temperature (°C), optimum coagulant dose (g/L) and pH. The average turbidity removal rates were approximately of 86% with abatement rates up to 95% like for Trigonella foenumgraecum and Abelmoschus esculentus at pH 3.17-3.20 (Khoo et al., 2021;Mohammad Lanan et al., 2020), and up to 77% for Tacca leontopetaloides at pH 3 (Makhtar et al., 2021), even though the considered pH values made water not immediately suitable for human consumption (WHO, 2007). Conversely, M. oleifera removed turbidity up to 97% at pH 6.8 (15 g/L) and up to 86-94% at pH 6.2 (0.15 mg/L) (Nhut et al., 2020;Vunain et al., 2019). Seeds of M. oleifera have been used as efficient natural coagulants in certain developing countries unaffordable for conventional chemicals (Bhatia et al., 2007). Its seeds can contain up to 34%, 15% and 16% of proteins, carbohydrates and lipids, in that order. (Othmani et al., 2020) suggested that the high amount of protein can be responsible of its great activity as coagulant.

Potentiality of plant-based coagulants to remove cyanobacteria
Currently, few studies have been reported to mitigate Cyano-HABs with plant-based coagulants as summarized in Table3 Results demonstrated that this plant-based coagulant can remove ~ 80% of M. aeruginosa cells. Camacho et al. (2015) explored the potential effect of M. oleifera at low turbidity level to sanitize water contaminated by cyanobacteria evidencing its ability to reduce chlorophyll-a and turbidity up to 60%, as well as suspended organic matter (40-50%). Thus, the removal of cyanobacteria and cyanotoxins in DWTPs can be carried out through two groups of methods: i) effective in removing intracellular cyanotoxin with intact cyanobacterial cells, and ii) eliminating extracellular cyanotoxin removing organic matter (Xagoraraki, 2007). To increase the whole performance of water treatment, reactions can occur sequentially in two separated reactors (Gitis and Hankins, 2018). Several treatment techniques are used in order to increase the performance of water treatment methods, e.g. photolysis with UV radiation at 254 and 185 nm (Chintalapati and Mohseni, 2020), adsorption process with activated carbons (Pendleton et al., 2001;Zhang et al., 2011) and hydrophyte filter bed (Song et al., 2009). Coagulation/ flocculation has been widely applied in combination with ultrafiltration, as an effective pre-treatment, to improve the removal of natural organic matter and to reduce membrane fouling (Liu et al., 2017). There is a great need to further research on the coagulation/flocculation process to identify the best practice to reduce effects of CyanoHABs considering also low tech-content methods. (Sillanpää et al., 2018) evidenced that the use of plantbased coagulants for the removal of suspended particles and natural organic matter in WWTPs is still underexplored. Currently, most results are laboratory based focusing on    (Camacho et al., 2015) controlling water turbidity by studying the mechanism of these natural coagulants through charge interaction and bridging mechanism that is attributed to the pair nature of the treated water and plant-based coagulant tested. According to (Ang and Mohammad, 2020), natural coagulants can record poor removal performance when the treated water contains many constituents such as suspended solids, heavy metals and microalgae, thus requiring several combined processes in order to meet the expected goal. Several studies (Choudhary et al., 2019a;Vunain et al., 2019;Wan et al., 2019) highlighted that plant-based coagulants have been used in various types of effluents saturated with different suspended solids ranging from wastewater, water from paint factories and artificially turbid water. The originality of the adoption of plant-based coagulants is related to the potential sources supplying the reagents like plant, including invasive species, or weeds (i.e., including seaweed), and plant waste. Some direct critical aspects in the use of plant-based coagulants are i) the lack of plants for mass processing; ii) the perception of a low-volume market; and iii) the lack of regulations stipulating the quality of processed coagulant extracts (Sutherland et al., 2002); iv) storage can be affected by microbial degradation causing undesired loss of reagents (Albaliwano et al., 2003;SAMIA et al., 1979).

A critical view on the applicability and future challenges of plant-based coagulants
In term of commercialization, few natural coagulants have reached the market, although several various native plant extracts have been identified as suitable for coagulation activities in removing turbidity and cyanobacteria (Sowmeyan et al., 2011). Currently, only M. oleifera seeds extracts are well documented with full-scale application in coagulation processes (Sutherland et al., 2002). Some critical points can affect the future employ of plant-based coagulants like the regular supply of raw materials mainly due to the relative economy of scale. For example, M. oleifera seeds can be harvested twice a year (Radovich, 2009) and there are still no clear estimate if the expected production will satisfy the possibility of a whole replacement of traditional chemical coagulants, or can represent just an integration and/or a partial substitution, greening just part of the process.
Another potential drawback identified from plant-based coagulants is the increase of organic load in the treated mass of water, as chemical oxygen demand (COD) and biological oxygen demand (BOD) (Sánchez-Martín et al., 2012), that can further promote microbial growth and potentially increase the frequency in clogging at the filtration stage of DWTPs. As a result, increased COD level can be a disadvantage if treated water is stored for a long period of time or requires chlorination (Sánchez-Martín et al., 2012). Distilled water extracts from M. oleifera (1%) can contain approximately 88.8 g/L of COD (Baptista et al., 2015), while the saline extraction up to 175 g/L.

Conclusions
Plant-based coagulants in DWTPs are an interesting and promising approach for the water sector that must be attentively evaluated, especially to integrate traditional chemical reagents. For sure, they cannot be considered as an overnight solution, but a medium-term potential option for greening the processes of coagulation/flocculation and cyanobacterial bloom removal. Several flaws are currently present and are mainly associated not only to the lack of data about full-scale applications, but also to the potential increase in treated water COD, the limited availability of adequate plant biomass and its potential biodegradability during storage conditions. The main advantages are related to the ability to support coagulation/flocculation treatments with efficiencies quite like to traditional reagents including costs, that with the relative economy of scale, could be potentially further reduced. Future focused research activities must elucidate: i) suitable species in an agricultural production perspective; ii) cost-benefit analysis; and iii) full-scale potential applicability.

Conflicts of interest
The authors declare no conflict of interest.
Acknowledgements This research was partially funded by MAECI (Ministry of Foreign Affairs and International Cooperation, Italy) supporting scientific collaboration between the University Cadi Ayyad (Faculty of Sciences Semlalia Marrakech, Morocco) and University of Naples Federico II (Naples, Italy).
The constructive comments from the anonymous reviewers are gratefully acknowledged.
Authors' contributions WEB was involved in literature review, data analysis and paper drafting; GL helped in paper drafting and data analysis; MD and AO contributed to data analysis; AY helped in literature review; GL and GM were involved in paper drafting and conceptualization; LA contributed to literature and draft review; and ML helped in conceptualization. All authors read and approved the final manuscript.
Funding Open access funding provided by Università degli Studi di Napoli Federico II within the CRUI-CARE Agreement. The research activity received no specific funding.

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Ethics approval and consent to participate Not applicable.

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Availability of data and materials All data generated or analysed during this study are included in this published article.

Competing interests
The authors declare that they have no competing interests.
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