Lactic acid fermentation of human excreta for agricultural application

Journal of Environmental Management 206 (2018) 890e900

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Journal of Environmental Management journal homepage: www.elsevier.com/locate/jenvman

Review

Lactic acid fermentation of human excreta for agricultural application Nadejda Andreev a, *, Mariska Ronteltap a, Boris Boincean b, Piet N.L. Lens a a b

UNESCO-IHE Institute for Water Education, PO Box 3015, 2601 DA, Delft, The Netherlands Research Institute for Field Crops, Selectia, 28 Calea Ies¸ilor str, MD 3101 Balti, Moldavia

a r t i c l e i n f o

a b s t r a c t

Article history: Received 14 July 2017 Received in revised form 19 November 2017 Accepted 26 November 2017

Studies show that source separated human excreta have a fertilizing potential with benefits to plant growth and crop yield similar or exceeding that of mineral fertilizers. The main challenges in fertilizing with excreta are pathogens, and an increased risk of eutrophication of water bodies in case of runoff. This review shows that lactic acid fermentation of excreta reduces the amount of pathogens, minimizes the nutrient loss and inhibits the production of malodorous compounds, thus increasing its agricultural value. Pathogens (e.g., Enterobacteriacea, Staphylococcus and Clostridium) can be reduced by 7 log CFUg
1 during 7e10 days of fermentation. However, more resistant pathogens (e.g. Ascaris) are not always efficiently removed. Direct application of lacto-fermented faeces to agriculture may be constrained by incomplete decomposition, high concentrations of organic acids or insufficient hygienization. Posttreatment by adding biochar, vermi-composting, or thermophilic composting stabilizes and sanitizes the material. Pot and field experiments on soil conditioners obtained via lactic acid fermentation and post treatment steps (composting or biochar addition) demonstrated increased crop yield and growth, as well as improved soil quality, in comparison to unfertilized controls. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Lactic acid fermentation Combined lactic acid fermentation and composting Biochar Resource recycling

Contents 1. 2. 3.

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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 891 Nutrient and resource challenges in sanitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 891 Reuse potential of excreta in agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 892 3.1. Fertilizer value of human urine and faeces . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 892 3.2. Advantages and disadvantages of biochar application to agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 892 3.3. Anthrosols: historical land application of human excreta and biochar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 892 Challenges in agricultural reuse of excreta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 893 4.1. Pathogen reduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 893 4.2. Concerns related to excreta storage and agricultural application . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 893 Lactic acid fermentation of human excreta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 893 5.1. Transformations occurring during lactic acid fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 893 5.2. Lactic acid fermentation of urine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 894 5.3. Lactic acid fermentation of faeces . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 894 5.4. Limitations of lactic acid fermentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 895 Post treatment of lacto-fermented human excreta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 896 6.1. Thermophilic composting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 896 6.2. Vermi-composting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 897 6.3. Addition of biochar . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 897 Agricultural effects of lacto-fermented excreta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 897 7.1. Effects of lacto-fermented excreta on soil and plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 897 7.2. Fertilizing effects of the post-treatments (composting and biochar addition) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 897

* Corresponding author. E-mail address: [email protected] (N. Andreev). https://doi.org/10.1016/j.jenvman.2017.11.072 0301-4797/© 2017 Elsevier Ltd. All rights reserved.

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Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 898 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 898 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 898

1. Introduction Global population growth, intense urbanization, economic development, and climate change increase competition for water, energy and land. While the need to produce more food to feed for a growing population is well known, the worldwide degradation of soil and water is increasingly worrisome (Hoff, 2011). Energy can be obtained from renewable resources, but water and soil have no substitutes. Therefore, it is imperative to prevent their further degradation and restore their quality. Soil is currently lost 10e40 times faster than it is regenerated (Bai et al., 2008; Pimentel, 2006). For this reason, farmers must spend more on energy, without a corresponding increase in crop yield, thus negatively affecting the livelihood of poor populations, especially in the developing countries of Africa, Asia and Latin America, whose economies depend on agriculture. Erosion and desertification are increasing throughout the world, which declines agricultural production in India, Pakistan, Nepal, Iran, Jordan, Lebanon and Israel (Pfeiffer, 2006). In Africa, three quarters of farmland is affected by soil degradation due to erosion and nutrient depletion (Mihelcic et al., 2011). The loss of nutrients and organic matter is also a concern in Europe, where approximately 45% of soils have reached a low or very low organic matter content of 0e2% (Rusco et al., 2001). This depletion is particularly intense in the Mediterranean region, Southern and Eastern Europe, as well as for some countries in Western Europe (Jones et al., 2012; Virto et al., 2014). Freshwater resources around the globe also face degradation and scarcity. For a number of countries in Africa and the Middle East, water is becoming physically scarce, while for others (e.g. Latin America) it is economically scarce (Rijsberman, 2006). Sanitation is a major consumer and polluter of water resources (Gleick, 2003). Large volumes of drinking water are used to transport excreta, generating enormous amounts of wastewater which cannot be fully cleaned with existing conventional technology. This results in significant amounts of nutrients and organic matter being discharged into surface waters, especially since 90% of the wastewater is released without treatment. Reusing excreta in agriculture returns nutrients to the soil and reduces the pollution of freshwater resources and, thus, the energy costs required for its treatment. Approximately one third of nitrogen, phosphorus and potassium fertilizer equivalents required by the farmers at the global level can be recovered from sanitation waste (Werner et al., 2003). Phosphorus reuse from sanitation is of particular interest, considering the projected increase in the price of phosphorous fertilizers. Mineral reserves are getting depleted, the geopolitical distribution is uneven, and the energy costs for mining, processing and extraction are increasing (Cordell and White, 2011). Prehistoric human societies have created long-lasting rich fertile soils by integrating their excrement, biochar and other substances into the ground (Lehmann et al., 2003). This occurred in the Amazon (terra preta or Amazonian dark earths; Glaser and Birk, 2012), Northern Europe (Wiedner et al., 2015), Australia (Downie et al., 2011), and West Africa (Frausin et al., 2014). This ancient practice of forming so-called terra preta soils highlights the potential for application of excreta and biochar for improving the soil fertility. In addition, with increased appreciation of the damage

caused to the environment and human health by the use of agrochemicals, there is more demand for organic production (Chojnacka, 2015). In this regard, lactic acid fermentation receives increased attention for its potential to substitute petroleumderived chemicals with biodegradable bio-based products, thus reducing greenhouse gas emissions and increasing the security of raw material supply (Daful et al., 2016; Ghaffar et al., 2014). The use of organic wastes for industrial production of organic acids (e.g. lactic acid) is becoming increasingly interesting due to low material costs (Couto, 2008). Among these, biodegradable polylactic acid has become of interest as it can replace synthetic plastics (Gavrilescu and Chisti, 2005). The anaerobic process of lactic acid fermentation (LAF) of manures and human excreata has recently received renewed attention as it is a key process in the resource-oriented approach, named “terra preta sanitation system” (Otterpohl and Buzie, 2013; ~ o, 2014), which treats excreta by Schuetze and Santiago-Fandin two combined processes: lactic acid fermentation (LAF), followed by composting (usually worm composting). Biochar is also applied to reduce nutrient losses and obtain stable organic soil conditioners (Bettendorf et al., 2014; Glaser and Birk, 2012; Yemaneh et al., 2014). Lactic acid fermentation contributes to controlling foul odour (Yemaneh et al., 2014) and suppresses the growth of pathogenic bacteria (Scheinemann et al., 2015). It is also shortens the required stabilization time during the subsequent vermicomposting stage (with earthworms), where further pathogen reduction, fragmentation and aeration occur in the faeces (Otterpohl and Buzie, 2013). This review evaluates the efficiency of the anaerobic process LAF, followed by vermi-composting and thermophilic composting in treating human excreta to improve their agricultural value. The role of biochar for avoiding nutrient loss and contributing to the formation of humus is highlighted and the potential fertilizing effects of excreta treated via LAF combined with composting and biochar addition are overviewed. 2. Nutrient and resource challenges in sanitation Conventional water-based sanitation aims to increase hygiene, but it is not applicable in all the societies of the world. Clean drinking water is used to transport excrement and is then treated via energy-intensive processes, but is never 100% clean again (Fig. 1, I). This is inappropriate, especially in regions with scarcity of freshwater or energy resources, which are growing due to droughts caused by global climate change (Hanjra and Qureshi, 2010). Freshwater pollution increases the costs of potable water treatment, but the wastewater that contaminates it contains numerous valuable resources, such as nutrients and organic matter from the food people eat (Fig. 1: II), in addition to constituents of concern, including pathogens, pharmaceuticals, hormones and pesticides (III). Wastewater is centrally collected and transported to the treatment facilities (IV), where the pollutants are only partly removed (Muga and Mihelcic, 2008), in addition to getting mixed with industrial wastewater and stormwater (V) (Tchobanoglous et al., 2003). Even with advanced treatment, such as microfiltration and reverse osmosis (Watkinson et al., 2007), micropollutants (e.g., pesticides, phenol compounds, heavy metals,

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also provides other elements that plants require, including calcium, magnesium, and micro-nutrients (e.g., B, Cu, Zn, Mo, Fe, Co and Mn) (Kirchmann and Pettersson, 1994). Experiments with 15N and 32P labelling in potted barley plants showed a higher phosphorus and almost equivalent nitrogen uptake from human urine compared to the soluble phosphorus and nitrogen from mineral fertilizers. The nutrient concentration in faeces is comparable to that of urine. However, faeces account for a much smaller quantity than urine (approx.1/10) and many of the nutrients, especially nitrogen, are organically bound (Winker et al., 2009). Since the amount of N, K and S found in faecal compost covers only a part of the crops' needs, it can be used primarily as a P-rich organic soil supplement and conditioner (Winker et al., 2009). 3.2. Advantages and disadvantages of biochar application to agriculture Fig. 1. Resource and nutrient challenges in conventional sanitation. WTP - water treatment plant; WWTP - wastewater treatment plant.

pharmaceuticals and personal care products) cannot be fully removed (Tchobanoglous et al., 2003) and, thus, present a risk to aquatic organisms (Cirja et al., 2008) and people living downstream. At the same time, valuable resources, like nitrogen and phosphorus, are not efficiently recycled (Rosemarin, 2010). While part of them are recovered during the treatment process and reused in agriculture (Fig. 1: VI), another part is released into aquatic ecosystems, causing along with agricultural runoffs (VIII), eutrophication and impairment of water quality (VII) (Jianyao et al., 2010; Syers et al., 2011). One limitation of conventional waterborne sanitation is the high cost of maintenance and operation. Most developed countries have already confronted significant costs for modernizing and upgrading their sanitation infrastructure, but in developing countries, the scarcity of financial and human resources often renders large wastewater treatment facilities dysfunctional after only a few years of operation. For example, in 1990, the government of Thailand invested USD 1.5 billion in wastewater and treatment facilities, but only 40% were functioning properly shortly after their installation (Schertenleib, 2005). Concern also rises over finding sufficient land suitable for landfilling the sewage sludge resulting from wastenez et al., 2010). water treatment plants (Jime Most urban and peri-urban populations of Africa, Asia and Central America, as well as rural populations in Eastern Europe rely on pit latrines as their primary means of sanitation. This system is affordable for people in water-scarce areas and those with limited financial resources (Morella et al., 2009). They, however, contribute to serious contamination of groundwater, soil, and water with nutrients and pathogens, thus increasing the health risk of those using groundwater as a drinking water source (Graham and Polizzotto, 2013). In addition, pit latrines are not suitable for crowded areas, sensitive coastal areas, soils with rocky grounds or those with a high water table or are periodically flooded (Hurtado, 2005). The potential increase in the intensity of floods and rise of the groundwater level, as a result of climate change can make this type of sanitation less suitable for some areas, especially in coastal zones (Graham and Polizzotto, 2013). 3. Reuse potential of excreta in agriculture 3.1. Fertilizer value of human urine and faeces In human urine, nitrogen, phosphorous, potassium and sulphur are present in ionic forms that plants can readily assimilate. Urine

Biochar is obtained by heating biomass above 250  C in the absence or with only limited oxygen supply (pyrolysis). The product is distinguished from charcoal by the purpose of use - soil application or environmental management and not for heating or cooking (Lehmann and Joseph, 2009). Application of biochar to soils with or without compost and fertilizers has been recognized among viable strategies for efficient restoration of organic carbon (Lehmann et al., 2006). This is related to its longevity in the soil and thus its capacity to maintain stable soil organic matter (Lehmann et al., 2006). The production and application of biochar is not yet standardized. Currently the voluntary product standards are in place (e.g. European Biochar Certificate or The Biochar Standard of the International Biochar Initiative) and in some countries such as Germany, Austria, Switzerland and Italy, national legislations were developed (Meyer et al., 2017). Application of biochar has a number of positive effects on crops and soils, including increases in water-holding capacity (Abel et al., 2013), raising the soil's cation exchange capacity (CEC), retention of plant-available nutrients, improving plant resistance to diseases (Elad et al., 2010), and enhancing crop productivity (Lehmann and Joseph, 2009). Biochar may, however, have negative effects as well. Agricultural application of freshly produced biochar may have null or negative effects on soil and plants. This is caused by highly labile fractions of carbon that can lead to nitrogen immobilization and, therefore, to a reduction in crop growth and yield. To make use of freshly produced biochars productively, co-composting and enrichment with mineral or organic fertilizers is recommended (Schmidt et al., 2014). 3.3. Anthrosols: historical land application of human excreta and biochar The reuse of animal or human excreta in combination with biochar was successfully applied in the past to transform easily weathered sandy soils, poor in organic matter and plant-available nutrients into long-lasting, highly fertile lands. An example is the terra preta soil type in permanent pre-Columbian Indian settlements created as a result of surface deposition, slash and burn cultivation or soil enrichment practices, with the integration of waste materials, such as plant residues, human excreta and charred biomass (Erickson, 2003). Analysis of faecal-specific steroids revealed a high input of human excreta into these terra preta soils (Glaser and Birk, 2012). Recent studies have indicated the presence of soils analogous to terra preta in Northern Europe and Australia (Downie et al., 2011), where the local indigenous population had similar waste management and soil enrichment practices as those in South America.

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In Europe, anthrosols were formed from heath and grass, mixed with animal manure, human faeces and charcoal, which were deposited on sandy soils. In Australia, the disposal of charcoal from cooking improved the soil's physical and chemical properties, including nutrient status, cation exchange capacity, and waterholding capacity. All these studies suggest that charcoal in combination with excreta created favourable conditions for maintaining soil fertility over long periods of times during ancient times and this practice can be applied today to restore soils around the world. 4. Challenges in agricultural reuse of excreta 4.1. Pathogen reduction One of the main challenges for excreta application in agriculture is the risk of infecting people with disease via contaminated food crops. In human urine the number of pathogens is usually low, however, in urine-diverting toilets cross-contamination is difficult to avoid. A study carried out in Sweden showed that 22% of the samples collected from urine tanks were contaminated with faeces €glund et al., 2002). (Ho Due to the potentially high amounts of pathogens, faeces have always been considered contagious and handled accordingly, since poor excreta sanitation may lead to the spread of disease (WHO, 2006). For example, in Vietnam, fertilization of farmlands with fresh or partially composted faecal waste from latrines caused up to 30% of hookworm infection among the local population and high indices of parasites like Ascaris, Trichurus and Taenia (Jensen et al., 2005). Depending on the local climate, storage during at least 1e6 months for urine and 1e2 years for faeces are recommended for pathogen removal (WHO, 2006). According to the WHO, in order to reduce the pathogens in human excreta to a safe level, a moisture content below 25% and a pH > 9 shall be ensured. In real life situations, such conditions of low moisture content and high pH can rarely be achieved. Moisture levels below 25% limits the activity of decomposing bacteria and fungi (Anderson et al., 1979) and the faecal material during storage is therefore more dehydrated than decomposed. During the last years, anaerobic digestion is used for hygienic treatment of excreta (Avery et al., 2014), however, the pathogen inactivation rate depends on the retention time. At 10e20  C, 75% of Ascaris suum eggs remained viable. A longer retention time (61e87 days) can lead to their complete destruction (Avery et al., 2014). Composting is an effective method for sanitizing sourceseparated faeces. It does, however, need to be mixed with organic waste, like vegetable scraps, at different ratios (Niwagaba et al., 2009). A sanitizing temperature above 50  C can be achieved and maintained for a sufficient number of days in stored faeces, if equal amounts of faeces and food waste are mixed (Niwagaba et al., 2009), which reduces by 3 log CFUg
1 and 4 log CFU g
1, respectively E. coli and Enterococcus. In addition, good insulation (e.g., 25e75 mm styrofoam), frequent turning and moisture levels below 65% are required. The main mechanisms responsible for pathogen reduction during composting are: thermal destruction, competition between indigenous and pathogenic microorganisms, antibiotic activity of fungi and actinomycetes and natural die-off (de Bertoldi et al., 1983; Haug, 1993). Thermal destruction plays an important role in the reduction of the viability of even most resistant pathogens such as Ascaris (Vinnerås et al., 2003). Another way to reduce the pathogens present in faeces is via vermi-composting. The mechanisms by which earthworms contribute to the reduction of pathogens are not clearly described. Coliform bacteria were significantly reduced in pig slurry in comparison to the control at low doses only (approximately 1 g of slurry

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to 1.5 g of earthworms per day), while at a higher dose (3 g slurry: 1.5 g of earthworms per day) it did not reduce their number significantly (Monroy et al., 2009). However, an efficient reduction of E. coli, Salmonella and Ascaris was achieved only with a high stocking density (of approximately 1: 1.5) earthworm biomass to biosolid ratio (Eastman et al., 2001), which is as much as 40 kg of earthworms to 60 kg of biosolid, an option which is not economically feasible in all cases. 4.2. Concerns related to excreta storage and agricultural application During extended storage and aerobic decomposition of faeces, up to 94% of the nitrogen and a significant amount of the carbon can be released to the atmosphere (Hotta and Funamizu, 2007). Up to 92% of the ammonia can be released during composting (Eghball et al., 1997), with the highest ammonia volatilization being encountered during the thermophilic phase of composting, where intensive mineralization takes place (Hao et al., 2011). A significant portion of organic matter (e.g., up to 62%) is lost as CO2 during the bio-oxidative stage of composting (Bernal et al., 1996). During vermi-composting, most of the nitrogen is emitted as N2O due to incomplete denitrification processes that occur in the guts of the earthworms (Frederickson and Howell, 2003). The variations in the nitrogen and organic matter loss depend on the time required for decomposition of the organic waste. Urine storage also leads to nutrient loss. Under the influence of urease-positive bacteria and free urease, urea is degraded to ammonia (NHþ 4 ) (Udert et al., 2006), part of which is lost during storage, transportation and field application (Rodhe et al., 2004). Urine hydrolysis also facilitates the precipitation of phosphates and carbonates, which are deposited at the bottom of the collection tanks (Udert et al., 2003). Repeated application of stored urine to the soil can also cause an increase in soil electric conductivity and salinization, due to its salt bearing ions (Naþ, Cl
, Ca2þ, Mg2þ and SO2
4 ) (Yongha Boh and Sauerborn, 2014). Urea degradation during urine storage can lead to a threefold-increase in urine salinity (Beler-Baykal et al., 2011). Ammonia and other malodorous compounds (e.g. VFA, indolic and phenolic compounds) formed during organic decomposition cause an undesirable odour of the stored urine (Troccaz et al., 2013; Zhang et al., 2013), which might be of a big concern during agricultural applications. Chemical acidification prevents volatilization of nitrogen, thus increasing the fertilizing value of excreta. For example, an acidified cattle manure slurry had 26% more nitrogen than a non-acidified one (Kosmalska, 2012). Besides reducing the NH3 loss, acidification of the slurry substantially reduces CH4 emissions as well (Petersen et al., 2012). However, this method is costly compared to the value of the nitrogen that is retained (Kirchmann, 1994). Acidification with sulphuric acid can cause H2S emissions and may negatively impact the soil by raising its electric conductivity (Frost et al., 1990). In addition, acid treatment may cause an increase in the concentrations of volatile fatty acids and volatile sulfurous compounds that may add to an overall increase in odour emissions (Petersen et al., 2012). Therefore, lowering the pH value can be a promising possibility for reducing gaseous emissions in excreta, however chemical acidification may be undesirable due to potential environmental concerns and odour intensification. 5. Lactic acid fermentation of human excreta 5.1. Transformations occurring during lactic acid fermentation LAF has been widely applied in food and silage preservation and treatment of kitchen and agricultural waste as well as animal

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manure (Kamra et al., 1984; Murphy et al., 2007; Wang et al., 2001). The use of LAF for treatment of human excreta has been extensively studied within the terra preta sanitation approach (Schuetze and Santiago-Fandino, 2014; Yemaneh et al., 2014). With a sufficient amount of organic acids, acidification takes place, which prevents the degradation of proteins. For example, the protein content did not change significantly after 10 days of lactofermentation of poultry manure with 10% of molasses and 3% of lactic acid bacterial inoculum (El-Jalil et al., 2008). In another study on a corn-chicken litter mixture, the total nitrogen and crude protein content did not change significantly even after 80 days of ensiling (Caswell et al., 1977). Also, treatment of manure with acidic liquid bio-waste from the milk and citrus industries decreased the pH to 5, reducing the CH4, N2O and NH3 emissions by 76e78%, 36e37% and 84e86%, respectively (Clemens et al., 2002; Samer et al., 2014). LAF contributes to the reduction of pathogens in excreta (Scheinemann et al., 2015), but its efficiency is still insufficiently investigated. This depends on the source of carbohydrates and the duration of the fermentation. LAF of faecal sludge and manure contributed to effective pathogen reduction, with the addition of molasses and wheat bran (10e12%) as sources of soluble carbohydrates (McCaskey and Wang, 1985; Scheinemann et al., 2015). LAF of swine manure decreased the Enterobacteriacea, Staphylococcus and Clostridium populations by 7 log CFU/g within a 7e10 days incubation, while the pathogeneity of Ascaris suum was completely lost after 56 days, its viability was already reduced after 21 days (Scheinemann et al., 2015). In a study on swine manure, Ascaris suum eggs remained infective even after 56 days of fermentation, even though their viability was considerably reduced (Caballerondez et al., 2004). Further investigations are required on Herna the efficacy of combined LAF and thermophilic composting or vermicomposting for the treatment of faeces. Protein complexes like bacteriocins and other compounds, including glucose oxidase, hydrogen peroxide and exopolysaccharides, have also a suppressive effect on pathogenic microorganisms (Saranraj, 2014). The mechanisms of the reduction of helminth eggs are poorly described. One of the factors is the increased temperature (36e37  C) during fermentation (Scheinemann et al., 2015). As lactic acid fermentation does not induce a temperature increase and the process usually takes place at lower temperatures than those indicated above, it might be challenging to raise the temperature of the slurry sufficiently. One option is to perform lactic acid fermentation under direct sunlight or in dark barrels that increase temperature when exposed to the sun (Scheinemann et al., 2015). LAF also deodorizes the offensive odour of excreta, by elimination of foul-smelling ingredients produced during the microbiological degradation of proteins, e.g. S-compounds (H2S), Ncompounds (NH3, indole and scatole) and C-compounds (lower fatty acids) (Hata, 1982; Wang et al., 2001). Formation of volatile fatty acids, responsible for the odour production in faeces, is inhibited during the lactic acid fermentation process (Kamra et al., 1984; Yemaneh et al., 2012). After a few days of fermentation, the foul faecal odour is changed to a sour-silage-like one. Considering the results from studies on the reduction of foul odour emissions via LAF in faeces, it would be interesting to investigate the mechanisms of the reduction of odour emissions in urine. For example, it is known that the representative stale urine odour is caused by the emission of phenol, indol and sulphide compounds produced by a range of anaerobic bacteria, such as Echerichia fergusonii, Enterococcus faecalis, Citrobacter kaseri, Streptococcus agalacticae, and Morganella morganii (Troccaz et al., 2013). LAB inhibit the production of some of these malodorous compounds, however the mechanisms are still poorly understood (Wang et al., 2001).

5.2. Lactic acid fermentation of urine During storage, the urine pH increases rapidly up to 8e9, when most urea is hydrolyzed (Kirchmann and Pettersson, 1994). The hydrolyzed urine has a high buffering capacity, thus the soluble carbohydrate source and the LAB should be added to the storage tanks prior to urine starts to accumulate there (Andreev et al., 2017a). Non-hydrolyzed urine can be a good growth medium for lactic acid bacteria as it contains urea, amino acids and minerals
2
such as Kþ, Naþ, Mgþ, PO3
4 , SO4 and Cl , which are important for the growth of LAB (Udert et al., 2006). During the urine LAF, the LAB inhibit the bacterial urease, thus preventing urea hydrolysis and consequently reduce ammonia volatilization. For example, studies have shown that the urease activity is diminished at pH < 5 (Schneider and Kaltwasser, 1984). Further research on the application of lactic acid fermentation of urine is important considering the potential for reducing the pH, thus minimizing the ammonia loss and phosphorous precipitation as well as the associated consequences such as smell and pipe clogging. Urine LAF can further add to the reduction of pathogens that may result from faecal cross-contamination. The capacity of LAB to degrade micropollutants such as hormones, pharmaceuticals and pesticides excreted via urine, which can diffuse into the aquatic environment after urine application in agriculture need further investigation. Ensilage of corn grain mixed with chicken manure for a period of 80 days reduced significantly (p < 0.01) the concentration of sulfoquinoxaline (a veterinary medicine to treat coccidiosis) compared to its concentration prior to ensilage (Caswell et al., 1977). Some strains of LAB are effective in the decomposition of organophosphorus pesticides, using them as a source of carbon and phosphorus for the synthesis of the enzyme phosphatase (Zhang et al., 2014). Lacto-fermented urine can also be soaked on biochar for nutrient capturing (Schmidt et al., 2015). Acidified urine may be more effective for biochar charging because sorption of ammonia and phosphate onto biochar is higher at lower pH (Yao et al., 2011). For example, phosphate adsorption was maximal at pH 2 to 4.1 and decreased at pH above 6 (Yao et al., 2011). The organic compounds in the urine are adsorbed on the biochar surface, forming an organic coating onto which anions and cations present in urine (e.g. phosphates and ammonium) can bind (Schmidt et al., 2015). 5.3. Lactic acid fermentation of faeces Fresh human faeces contain only a low number of microbial species facilitating lactic acid fermentation, thus the addition of LAB and an appropriate substrate favouring their growth is required (Otterpohl and Buzie, 2013). The use of lactobacilli strains such as Lactobacillus plantarum, Lactobacillus casei and Pediococcus acidilactici as additives promotes lactic acid fermentation of faeces (Yemaneh et al., 2012). Low cost sources of lactic acid bacteria are waste products of milk and grains. The excreted carbohydrate fraction in faeces is usually composed of undigested cellulose, vegetable fiber, oligosaccharides and polysaccharides, not hydrolyzed by the digestive system of humans (Southgate and Durnin, 1970). Soluble carbohydrates to be added to faeces can be found in molasses, whey or waste from starchy materials such as potato, wheat, manioc or barley (Pandey et al., 2000). A potential cheap source of soluble carbohydrates that can be added to the cover material for faeces dehydration is press mud, a discarded product from beet sugar industry, that currently has no monetary value, despite its content of 5e15% sugar (Partha and Sivasubramanian, 2006). Press mud addition is important if lactic acid fermentation is followed by vermi-composting, as it is easily processed by earthworms (Prakash and Karmegam, 2010). The

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application of biochar as a cover material in dry toilets with mixed collection of urine and faeces showed a 2.3 and 1.7 times lower carbon loss and 1.9 and 1.3 lower nitrogen loss than rice husk and corn stalk, respectively (Hijikata et al., 2015). Since the pH of the biochar is mostly alkaline, its addition at the end of the lactic acid fermentation or at the post-treatment stage (thermophilic or vermi-composting) is more appropriate. The quantity of source separated faeces and toilet paper generated per capita per year is relatively low, approximately, 70 kg and 6 kg (wet weight) per year, respectively (Rose et al., 2015). After the collection stage, faeces and toilet paper could be treated via extended LAF along with other types of organic material such as kitchen/food industrial waste (e.g. fruit, milk or sugar industry wastes) or animal manure (Fig. 2). Vegetable waste is rich in LAB, enzymes (e.g. cellulolytic, lignolytic and pectinolytic) and carbohydrates (Jawad et al., 2013) and can speed up the LAF of faeces and cover material as well as of the thermophilic stage of composting, thus shortening the overall time required for the treatment of faeces. Pre-fermenting (simple storage in closed vessels) of kitchen and fruit waste prior to being mixed with the faeces will release the sugars by the activity of extracellular enzymes and facilitate a better fermentation of faeces. Alternatively, addition of cattle or swine manure to human faeces during secondary faeces treatment is beneficial owing to a higher number of lactic, cellulolytic and hemicellulolytic bacteria that are capable of fermenting a range of

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monosaccharides, oligosaccharides, polysaccharides and lignocelluloses (Dowd et al., 2008). These cellulolytic and hemicellulolytic bacteria, e.g. Clostridia and Ruminococcus, might be important for an effective decomposition of lignin and cellulose from toilet paper and sawdust in the cover material.

5.4. Limitations of lactic acid fermentation Among the main limitations of LAF is the need for creating an enabling environment for the optimal growth of LAB, promoting acidification and stabilization of excreta, including inoculation of LAB nutritional additives like sources of carbon (Saeed and Salam, 2013). The nature of the added components (e.g. kitchen, waste from food industry or cattle manure) as well as the interactions between different lactic acid bacteria strains and fungi during the storage and fermentation process may also influence the efficiency of the lactic acid fermentation as well as combined lactic acid fermentation and thermophilic or vermi-composting processes. Comprehensive studies on these aspects are currently lacking. Another limitation is that an effective acidification of faeces or sewage sludge is obtained only with the addition of sources of easily fermentable carbohydrates such as molasses or wheat bran (Yemaneh et al., 2012). These may have other potential competitive uses in the fermentation industry (Dumbrepatil et al., 2008; Javed et al., 2012). Therefore, it is important to identify non-value waste

Fig. 2. Overview of the potential steps and additives used during lactic acid fermentation of the urine and faeces fraction of urine diverting systems. LAB - lactic acid bacteria, SCsoluble carbohydrates.

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materials rich in sugar and starch, such as kitchen and food industry waste, to be used in lactic acid fermentation (Yemaneh et al., 2014). 6. Post treatment of lacto-fermented human excreta LAF of faeces contributes to the reduction of pathogens and odour (Scheinemann et al., 2015; Yemaneh et al., 2014). However, its direct application to the soil may create some problems. There are a number of constrains for soil application (Fig. 3): the lactofermented faeces may not always be fully sanitized (Buzie and €rner, 2014), they are anaerobic and rich in organic acids, thus Ko their addition to the soil may intensify the mineralization of soil organic matter (Hamer and Marschner, 2005). Therefore, before being applied to the soil, the lacto-fermented faeces can be either mixed with biochar or processed further via thermophilic or vermi-composting. 6.1. Thermophilic composting In order to improve the structure and stabilize the anaerobic lacto-fermented substrate, the LAF stage can be combined with thermophilic composting (Andreev et al., 2017b). The presence of labile forms of carbon in the initial material (caused for example, by the addition of molasses) contributes to a reduction of ammonia volatilization due to immobilization of the NHþ 4 -N by the microbial

biomass (Liang et al., 2006). During the transition from the mesophilic to the thermophilic stage, an increase in organic acids and a low pH usually leads to a stagnation or decline in microbial activity, thus slowing down the bio-degradation process (Sundberg et al., 2004). However, addition of molasses may stimulate growth of acid-tolerant thermophilic bacteria (Thian, 2015) which can accelerate the composting process. Therefore, treating of excreta via LAF contributed to a rapid increase in thermophilic temperature above 55  C without turning and mixing (Andreev et al., 2017b), while in simple composting the temperature remained below 40  C. The overall composting period lasted for only 23 days in comparison to composting that lasted for 33 days (Andreev et al., 2017b). Integrating the processes of LAF with thermophilic composting was more efficient in the reduction of coliform bacteria and E. faecalis as well as plant growth and germination than combining LAF with vermi-composting (Andreev et al., 2017b). This might be related to the fact that during LAF, lactic acid bacteria produce substances with antagonistic effects on pathogens. Such a substance is for example bacteriocin that is thermoresistant and inhibits a wide range of pathogens. The bacteriocin can however be broken down by proteases produced in high amounts during vermi-composting (Abo-Amer, 2007; Devi et al., 2009). Combining LAF with thermophilic composting employs a faster turnover (approximately one month) in contrast to vermi-composting, which takes longer, i.e. 4 months (Andreev et al., 2017b). The thermophilic phase of composting, which will follow the

Fig. 3. Effects of lactic acid fermentation and post-treatment of human faeces.

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LAF process, will contribute to decomposition of more slowly degradable materials such as celluloses and hemicelluloses by facultative thermophilic anaerobes, i.e. Clostridia. The cellulolytic enzyme system of these bacteria works optimally in low oxygen conditions (below 2%) and higher temperatures of 50e60  C (Schwarz, 2001). 6.2. Vermi-composting Vermi-composted material has a better structure as the earthworms are mixing and grinding the substrate, thus increasing nutrient availability and the content of humic substances (Fig. 2). The mineralization activity of bacteria and fungi that populate the earthworm gut release plant available nutrients, including N, P, K and trace elements (Zn, Mn and Fe) (Yadav and Garg, 2011). One limitation of this treatment is that the lacto-fermented faeces needs to be ventilated for at least 72 h or mixed with a bulking material such as vermi-compost, cattle manure or biochar prior to inocula€ rner, 2014). Limited oxygen tion with earthworms (Buzie and Ko supply in the lacto-fermented material may be detrimental to earthworms as they die very quickly in anaerobic conditions (Munroe, 2007). Vermi-composting generates high N2O emissions from the worms themselves and their casts. Pre-treatment of faeces with kitchen waste via lactic acid fermentation releases large amounts of sugars, organic acids and amino acids. These can serve as electron donors for nitrate reduction in the gut of earthworms and can thus lead to more intense N2O emissions in the course of incomplete denitrification (Asuming-Brempong and Nyalemegbe, 2014). 6.3. Addition of biochar Biochar has a high surface area (Jindo et al., 2012) and adsorbs
NH3, NHþ 4 and NO3 , thus preventing their loss via volatilization or leaching. By creating a favourable microenvironment for nitrifying bacteria (Jindo et al., 2012) it also promotes nitrification. Biochar particles further improve the texture of the lacto-fermented material by improving aeration (Jindo et al., 2012). Biochar addition at the vermi-composting or thermophilic composting stage is important for increasing the stability of the compost, reducing the nutrient loss and improving the compost structure. The high temperature (±70  C) generated by aerobic thermophilic composting further adds to surface oxidation and an increase in the acidic functional groups, thus enhancing the biochar capacity to absorb nutrients and dissolved organic matter (Cheng et al., 2006). A high degree of humus formation was observed upon the addition of only 2% dry weight of biochar to compost (Jindo et al., 2012). 7. Agricultural effects of lacto-fermented excreta 7.1. Effects of lacto-fermented excreta on soil and plants Application of lacto-fermented urine may be advantageous over simple stored urine as the reduced pH of lacto-fermented urine reduces the risk of ammonia loss (Andreev et al., 2017a) and its salinity due to urea inhibition (Yongha Boh and Sauerborn, 2014). Research on the agricultural effects of lacto-fermented human excreta is rather scarce. The benefits reported are mainly from related studies on bokashi (anaerobically fermented animal manure or vegetable waste with rice bran and microbial inoculum containing LAB). These benefits include: a) increased growth, yield and quality of crops; b) increment in nutrient availability (e.g. phosphorus) as LAB are able to solubilize insoluble phosphates in compost and also from the soil (Zlotnikov et al., 2013), through

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production of organic acids, phosphatase enzymes and reduction of pH.; c) enhanced soil biological activity; d) improved physical properties of soil and e) suppressed plant pathogens. Table 1 overviews the main effects of lacto-fermented human and animal excreta and vegetable waste on soils and crops. In a two year field experiment, lacto-fermented faeces and organic waste, supplemented with biochar that had been soaked in urine significantly improved (p < 0.05) the yield of corn on a clay-loamy chernoziom in Moldova compared to the unfertilized control, aged cattle manure, faeces, urine and vermicast obtained via LAF combined with vermi-composting (Andreev et al., 2016). In contrast, the mineral fertilizer led to a significantly lower corn yield during the first production year and a not significantly different yield during the second production year. The lacto-fermented mix supplemented with biochar also significantly reduced the soil bulk density and increased the mobile potassium content in comparison to the control and other fertilizers (Andreev et al., 2016). The application of lacto-fermented kitchen scraps produced corn plants that were twice taller (p < 0.05) and had more leaves than the control (Alattar et al., 2016). Fermented vegetable waste with wheat bran and inoculum improved the nutrient availability, but produced a 29% lower tomato yield than a mineral fertilizer mixed with the same inoculum (Hui-Lian et al., 2001). The quality of the fruits, i.e. sugar, organic acid and vitamin C content, was, however, higher in the plants that were fertilized with the fermented organic waste. Tomato plants growing in soil inoculated with LAB had 2e4 fold more fresh weight of fruits than the control plants (Hoda et al., 2011). LAB also benefit the growth and yield of crops. The addition of lacto-fermented material alters the biology, physics and chemistry of the soil due to the activity of LAB themselves or the compounds they produce. Carbohydrates, amino acids, organic acids and other metabolites produced by LAB may stimulate beneficial soil microorganisms and suppress plant pathogens (Hoda et al., 2011). For example, the disease incidence of bacterial wilt (by Ralstonia solanacerum) was reduced by 63% in tomato (Murthy et al., 2012) and damage from bacterial infections by Pseudomonas (number of lesions per leaf and percentage of dead leaves; p < 0.05) was significantly reduced in bean plants compared to the control (Visser et al., 1986). 7.2. Fertilizing effects of the post-treatments (composting and biochar addition) Pot experiments with faeces from dry toilets, with mixed collection of faeces and urine, where biochar was used as a cover material during the collection stage, significantly increased the growth of mustard spinach Brassica rapa compared to ambient sandy soil (Hijikata et al., 2015). The authors related this growth increase to the biochar contribution to NO
3 retention, leading to increased nitrification rates as well as preventing its loss via leaching. Compost with 2% wet weight of biochar improved up to 5 times more growth of Chenopodium quinoa (Kammann et al., 2015). In another study, biochar amended compost contributed to increased water retention, nutrient uptake by plants and crop yield (Agegnehu et al., 2015). Additional research is still needed to clarify the role of biochar in capturing the nutrients from urine and faeces and their release to the soil and plants. For example, pumpkin plants fertilized with biochar soaked in cow urine had a threefold higher yield compared to plants fertilized with urine alone (Schmidt et al., 2015). In addition, in a field experiment on a tropical Andosol, a fertilizer composed of co-composed pasteurized faeces, mineral additives (i.e. ash and brick particles), kitchen waste, urine and biochar gave a 16% increase in corn yield compared to an unfertilized control. It

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Table 1 Overview of the main effects on soil and plants after application of lacto-fermented faeces, combined lacto-fermented and composted organic waste and charcoal. Plants used

Effects on soil and crops

Reference

Experimental conditions

Soil type, geographical location and scale of the experiment

Source separated faeces and biowaste (manure, kitchen waste) was lacto-fermented with sugar beet molasses and bacterial innoculum from sauerkraut in earth pits lined and covered with plastic foil for 8 weeks. Before field application, the lacto-fermented mix was supplemented with urine charged biochar. For the second production year, the lacto-fermented mix supplemented by biochar was also vermicomposted.

Corn (Zea Clay loamy chernoziom, Eastern Europe, Moldova, mays) Two year field experiments

Andreev et al., 2016

Bokashi (Rice bran, rice husk, rapeseeds oil mill sludge, fish meal anaerobically fermented with Lactobacillus and yeast), application rate 3000 kg/ha compared to NPK fertilizer (15:15:15) at a rate of 600 kg/ha Bokashi was obtained by fermenting fruit waste, grass weeds with mollases and effective microorganisms in a closed bucket for a period of 10 days. Comparison was made with bokashi without EM and control of farmer practice.

Field experiments 42 m2 each plot

Pei-Sheng and HuiLian, 2002

Field experiments on a 197.4 m2 area.

also increased the soil available phosphorous from 0.5 to 4.4 mg kg
1 and the soil pH from 5.3 to 5.9, thus reducing acidification (Krause et al., 2015). 8. Conclusions The potential of LAF as alternative anaerobic treatment of manure and excreta for organic matter stabilization, reducing pathogens, preventing nutrient losses and odour control has been reviewed. The combination of LAF with composting (thermophilic composting or vermicomposting) and biochar addition further stabilizes the organic matter and improves hygienization. The main limitations of LAF of excreta is the need to provide an enabling environment for lactic acid bacteria, i.e. addition of easily fermentable carbohydrate sources as molasses or wheat bran. Agricultural studies on the effects of applying lacto-fermented excreta demonstrate potential benefits on both crop production and soil quality. Acknowledgements The authors acknowledge the Nuffic NFP fellowship program (grant number CF8080) for providing financial support for undertaking this review study. Many thanks to Christopher Canaday,  n Omaere (Puyo, Ecuador) for proofreading biologist at the Fundacio the manuscript and providing valuable comments for its improvement. References Abel, S., Peters, A., Trinks, S., Schonsky, H., Facklam, M., Wessolek, G., 2013. Impact of biochar and hydrochar addition on water retention and water repellency of sandy soil. Geoderma 202, 183e191. Abo-Amer, A.E., 2007. Characterization of a bacteriocin-like inhibitory substance produced by Lactobacillus plantarum isolated from Egyptian home-made yogurt. Sci. Asia 33, 313e319. Agegnehu, G., Bird, M., Nelson, P., Bass, A., 2015. The ameliorating effects of biochar on soil quality and plant growth on a ferrasol. Soil Res. 53, 1e22. Alattar, M.A., Alattar, F.N., Popa, R., 2016. Effects of microaerobic fermentation and black soldier fly larvae food scrap processing residues on the growth of corn plants (Zea mays). Plant Sci. Today 3, 57e62. Anderson, D., Greig-Smith, P., Pitelka, F., 1979. The influence of physico-chemical environment on decomposition process. In: Anderson, D., Greig-Smith, P., Pitelka, F. (Eds.), Decomposition in Terrestrial Ecosystems. Blackwell Scientific Publications, University of California Press, Great Yarmouth, Norfolk. Andreev, N., Ronteltap, M., Lens, P., Boincean, B., Bulat, L., Zubcov, E., 2016. Lactofermented mix of faeces and bio-waste supplemented by biochar improves the

The corn yield was significantly higher than the control, stored cattle manure, faeces, urine and vermicomposted lacto-fermented mix. In relation to mineral fertilizer, a significantly higher yield was produced during first production year and a not significant different yield during the second production year. Lacto-fermented mix supplemented by biochar had also lowered soil bulk density and enhanced soil potassium content in relation to the control and other fertilizers. Fresh weight of nodules on lateral plants, the pod numbers Peanut (Arachis with two seed and yield in plants fertilized by EM bokashi hypogaea was significantly higher than in those fertilized by chemical fertilizer L.) Corn Zea Plants fertilized by EM bokashi were two times taller and mays L. had 14% more leaves

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