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This factsheet presents the planning and implementation of the Xavier Ecoville (XE), located in Lumbia, in the city district of Cagayan de Oro (Northern Mindanao, Philippines). This factsheet puts a special focus on education, organisation and implementation concerning WASH services in the Ecoville. The XU SuSan Center works in collaboration with the SSWM Toolbox and has taken part in its development. General Introduction to the Philippine CultureThe Philippines is a country rich in human and natural resources, but also known as the oldest democracy in Asia.
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Animal Manures: Recycling and Management TechnologiesMaria Gomez-Brandon1, Marina Fernandez-Delgado Juarez 1, Heribert Insam1 and Jorge Dominguez2[1] University of Innsbruck, Institute of Microbiology, Innsbruck, Austria[2] Departamento de Ecoloxia e Bioloxia Animal, Facultade de Bioloxia, Universidade de Vigo, Vigo, Spain1. The Ecoville is a resettlement site donated by Xavier University-Ateneo de Cagayan (XU), housing for 550 families who lost their homes due to the aftermath of typhoon Sendong in December 2011. A WASH service programme has been developed in by the Sustainable Sanitation (SuSan) Center of XU, using the SSWM Toolbox approaches as a baseline. With the aftermath of typhoon Sendong and the building of the XU Ecoville, the bond and exchange of this cooperation has become even stronger. However, the country is facing many problems that stem from a high level of corruption and little state security (see also water corruption), and an underdeveloped domestic market that results in a high level of poverty as well as health and social hazards (REESE 2006). Changes in the microbial community structure throughout the process of vermicomposting assessed by the principal component analysis of the twenty-seven PLFAs identified in the layers of reactors fed with rabbit manure. Changes in (a) Gram-positive bacterial, (b) Gram-negative bacterial and (c) fungal PLFAs in the layers of reactors fed with rabbit manure throughout the process of vermicomposting.
Changes in (a) microbial activity assessed by basal respiration, and (b) dissolved organic carbon content in the layers of reactors fed with rabbit manure throughout the process of vermicomposting. Abundance of Escherichia coli and faecal coliforms in the original materials (manure (M), compost (C), vermicompost (Vc) and anaerobic digested slurry (AS)) and in the unamended and amended soils at the three incubation times (0, 15 and 60 days).
Abundance of Clostridium perfringens in the original materials (manure (M), compost (C), vermicompost (Vc) and anaerobic digested slurry (AS)) and in the unamended and amended soils at the three incubation times (0, 15 and 60 days). IntroductionMany environmental problems of current concern are due to the high production and local accumulations of organic wastes that are too great for the basic degradation processes inherent in nature. Furthermore, the SuSan Center is acting as secretariat of another XU project, called “Sustainable Sanitation and Health Program” (Convergence Project) aiming at improving health and sanitation services in this area through the implementation of ecological sanitation and nutrient recovery. This case study therefore can be seen as part of a mutual learning process through the implementation of an SSWM Project (SSWM Implementation Project). Concerning Philippines WASH services, the absence of a clear national regulatory framework in this sector combined with high poverty levels have led to the situation that less than 10% of Filipinos are currently connected to a sewage system, and most flush toilets work with a septic tank (DOH 2010). With adequate application rates, animal manure constitutes a valuable resource as a soil fertilizer, as it provides a high content of macro- and micronutrients for crop growth and represents a low-cost, environmentally- friendly alternative to mineral fertilizers [1]. A special focus is given to a multidisciplinary approach involving the different units (from health and social science to sustainable agriculture) of XU in the project. Natural hazards like tropical storms are a constant phenomenon on the more than 7000 islands, and constitute a large risk for the population and the already instable water and sanitation situation.More than 80% of the Philippine population are Roman Catholics, whilst around 5% are Muslims.
Different letters indicate significant differences between the layers based on post hoc test (Tukey HSD).
However, the intensification of animal husbandry has resulted in an increase in the production of manure - over 1500 million tonnes are produced yearly in the EU-27 [2] as reported by Holm-Nielsen et al. The Convergence Project, which has been implemented in Lumbia before the Ecoville was created, has now been interlinked with the activities at the Ecoville. Religion plays an important role in Philippine culture and is practised and shown regularly in everyday life. Families as well as communities are organised in strict hierarchies, and due to a lack of security concerning health care and income, it is common to live within strong family and community bonds (GIZ 2012).The Philippines consist of more than 7, 000 islands and are located in Southeast Asia.
Research studies focused on the stabilization of animal manures through the aerobic processes of composting and vermicomposting. In fact, the agricultural contribution to total greenhouse gas emissions is around 10%, with livestock playing a key role through methane emission from enteric fermentation and through manure production. More specifically, around 65% of anthropogenic N2O and 64% of anthropogenic NH3 emissions come from the worldwide animal production sector [5]. Source: ZECH (2011)Extension activities are the activities conducted by Xavier University faculty, staff and students outside the campus, extending help to the community, especially in Northern Mindanao. The introduction of appropriate management technologies could thus mitigate the health and environmental risks associated with the overproduction of organic wastes derived from the livestock industry by stabilizing them before their use or disposal. It is an aim of XU that any extension activities should be research-based or backed with research so that data collection and record keeping of activities and interventions are properly considered.
Stabilisation involves the decomposition of an organic material to the extent of eliminating the hazards and is normally reflected by decreases in microbial biomass and its activity and in concentrations of labile compounds [6]. Composting and vermicomposting have become two of the best-known environmentally appropriate technologies for the recycling of manures under aerobic conditions [6-7], by transforming them into safer and more stabilised products (compost and vermicompost) with benefits for both agriculture and the environment. Hundreds of families do not have access to basic sanitation facilities, including the access to safe water (see also access to water and sanitation), which is why the XU convergence project came into action. Unlike composting, vermicomposting depends on the joint action between earthworms and microorganisms and does not involve a thermophilic phase [8].
When typhoon Sendong hit the coast of Northern Mindanao in December 2011, thousands of people became homeless. However, more than a century had to pass before vermicomposting was truly considered a field of scientific knowledge or even a real technology, despite Darwin [9] having already highlighted the important role of earthworms in the decomposition of dead plants and the release of nutrients from them.
Although microbial degradation under oxygen is usually faster and, as such aerobic processes are thermodynamically more favorable than anaerobic processes, in recent years, anaerobic digestion (AD) has become an upcoming technology for the treatment of animal manures [3, 10-13].
On the one hand, pretreatment of manure by anaerobic digestion can involve some advantages including malodor reduction, decreased biochemical oxygen demand, pathogen control, along with a reduction in the net global warming potential of the manure [4,14]. It includes a new perspective of recognising human urine, faeces and wastewater not as waste, but as valuable resources. This process has other direct advantages beyond these, which are related to biogas production for renewable energy and the enrichment of mineral fractions of N and P during digestion [4,10], resulting in a more balanced nutrient mix and increased nutrient bioavalability for plants compared with undigested manure [15]. Sanitation is being closely linked to agriculture (see also the factsheets on the nutrient and water cycle; and linking up sustainable sanitation and agriculture).
Therefore, the purpose of this chapter is to give an overview of the three major management technologies of manure recycling, including the aerobic processes of composting and vermicomposting and the anaerobic digestion for biogas production. This link leads to the creation of added values in the form of food, income, better human health, and a cleaner environment (see also agricultural issues, sanitation and health and environmental issues).
The main changes that occur in the substrate from a chemical and microbial viewpoint during the specific phases of each degradation process are addressed, as such changes determine the degree of stability of the end product and in turn its safe use as an organic amendment.
The Convergence Project introduces and educates people about the holistic approach of sustainable sanitation and thereby helps them to adopt new practices.
It is also about generating economic benefits, which are helpful to individual households as well as to the sustainability of the project (see also sanitation and economy).
Also, the influence of the end products derived from each process on the soil microbiota and disease suppressiveness are discussed.2.
Moreover, the project promotes the application of scientifically-proven methods and findings into real life or - the other way around – the conduct of scientific research projects that are all relevant for the Sustainable Sanitation and Health Development Program. Aerobic degradation: Composting and vermicomposting processesUnder aerobic conditions, the degradation of organic matter is an exothermic process during which oxygen acts as a terminal electron acceptor and the organic materials are transformed into more stable products, carbon dioxide and water are released, and heat is evolved.
Under field conditions, aerobic degradation takes place slowly at the soil surface, without reaching high temperatures; but this natural breakdown process can be accelerated by heaping the material into windrows to avoid heat losses and thus allowing for temperature increases (composting) or by using specific species of earthworms as agents for turning, fragmentation, and aeration (vermicomposting). Although both aerobic processes, composting and vermicomposting, have been widely used for processing different types of animal manure either separately or in combination with each other (see Table 1), most of the studies are not comparable mainly due to differences in the applied experimental designs, parent material, earthworm species, as well as the length of the experiments and the parameters used for analysis, among others. Despite these limitations, all these findings have largely contributed to better understand the changes that the material undergoes during these biological stabilisation processes, which is of great importance for their optimisation, and ultimately to obtain a high quality final product. In line with this, certain chemical characteristics of the animal manures can limit the efficiency of these processes, such as an excess of moisture, low porosity, a high N concentration in relation to the organic C content or high pH values [6]. Source: SUSAN CENTER (2012)ActivitiesAll activities of the members are arranged according to a module system, which is based on the tasks identified. Therefore, different aeration strategies, substrate conditioning-feedstock formulation, bulking agents and process control options have been considered in manure composting and vermicomposting so as to reduce the time and costs of both processes and enhance the quality of the end-products [6-7]. The composting processComposting is defined as a bio-oxidative process involving the mineralization and partial humification of the organic matter, leading to a stabilised final product, free of phytotoxicity and pathogens and with certain humic properties, which can be used to improve and maintain soil quality and fertility [25].
Composting of animal manures has been traditionally carried out by the farmers after manure collection for better handling, transport and management [6]. Source: BBC (2011)Thousands of families in Cagayan de Oro (CDO) became homeless and lost all their belongings.
Frequently, the wastes were heaped up and very little attention was paid to the process conditions (aeration, temperature, ammonia loss, etc.) and using rudimentary methodology. Many of those are not allowed to return to their own areas anymore, since they were declared flood-prone areas.
Therefore, one of the major decisions XU has taken was to donate 5 of its 17 hectares of land in Lumbia in order to provide a place for a new settlement for the survivors. However, in general, composting may be described as a four-phase process in which the energy-rich, abundant and easily degradable compounds like sugars and proteins are degraded by fungi and bacteria (referred to as primary decomposers) during an initial phase called the mesophilic phase (25-40 ?C). Although there exists a competition between both microbial groups regarding the easily available substrates, fungi are very soon outcompeted because the maximum of specific growth rates of bacteria exceed those of fungi by one order of magnitude [26].
Since XE is located in Lumbia, it automatically became a part of the SS-HDP Convergence Project.XE DevelopmentSendong survivors living in XE come from different areas in CDO. The importance of bacteria (with the exception of Actinobacteria) during the composting process has long been neglected, probably because of the better visibility of mycelial organisms.
Provided that mechanical influences (like turning) are small, compost fauna including earthworms, mites and millipedes may also act as catalysts, thereby contributing to the mechanical breakdown and offering an intestinal habitat for specialized microorganisms. The contribution of these animals may be negligible or, as in the special case of vermicomposting, considerable (see section 2.2). Source: SUSAN CENTER (2012)ObjectivesXE is envisioned to become an ecologically friendly, self-reliant, God-centred community. The number of mesophilic organisms in the original substrate is three orders of magnitude higher than the number of thermophilic organisms; however, the activity of primary decomposers induces a temperature rise and in turn, mesophilic microbiota is, along with the remaining easily degradable compounds, degraded by the succeeding thermophiles. The temperature rise continues to be fast and accelerates up to a temperature of about 62 ?C during this second phase of composting, known as the thermophilic phase.
When a temperature exceeding 55 ?C is reached in a compost pile, fungal growth is usually inhibited and the thermophilic bacteria and Actinobacteria are the main degraders during this peak-heating phase. Moreover, oxygen supply affects fungi to a greater extent than bacteria, and even in force-aerated systems, temporary anoxic conditions may occur.

Hence, fungi play a negligible role during this phase, except for the composting of lignocellulosic residues. Bacteria of the genus Bacillus are often dominant when the temperature ranges from 50 to 65 ?C. A number of autotrophic bacteria that obtain their energy by the oxidation of sulfur or hydrogen have been isolated from composts [28]. Their temperature optimum is at 70-75 ?C and they closely resemble Hydrogenobacter strains, which were previously found in geothermal sites.
Furthermore, obligate anaerobic bacteria are also common in composts, but up to now, there is still a gap of knowledge concerning this microbial group. It is believed that the longer generation times of archaea, in comparison with bacteria, made the archaea unsuitable for the rapidly changing conditions in the composting process. Nevertheless, in recent works, and using the right tools, a considerable number of cultivable (Methanosarcina termophila, Methanothermobacter sp., Methanobacterium formicicum, among others) and yet uncultivated archaea have been detected in composting processes [29-30].
The final temperature increase may exceed 80 ?C and it is mainly due to the effect of abiotic exothermic reactions in which temperature-stable enzymes of Actinobacteria might be involved. This facilitates the coordination and development process of both projects.Heading the WASH team, the SuSan Center ensures that a comprehensive management for water, sanitation and hygiene is implemented at XE. Such high temperatures are crucial for compost hygienisation in order to destroy human and plant pathogens, and kill weed seeds and insect larvae [31]. From solid waste segregation to wastewater management, the Center has done an excellent job in responding to the WASH needs of XE. The disadvantage of temperatures exceeding 70 ?C is that most mesophiles are killed, and therefore the recovery of the decomposer community is retarded after the temperature peak. The inoculation with matter from the first mesophilic stage might, however, solve this problem.When the activity of thermophilic organisms ceases due to the exhaustion of substrates, the temperature starts to decrease. This constitutes the beginning of the third stage of composting, called the cooling phase or second mesophilic phase.
It is characterised by the recolonisation of the substrate with mesophilic organisms, either originating from surviving spores, through the spread from protected microniches, or from external inoculation. During this phase there is an increased number of organisms with the ability to degrade cellulose or starch, such as the bacteria Cellulomonas, Clostridium and Nocardia, and fungi of the genera Aspergillus, Fusarium and Paecilomyces [27].
Solid Waste ManagementProvision of collection bins for segregated collection of biodegradables and reusable inorganic material (e.g.
Finally, during the maturation phase, the ratio of fungi to bacteria increases due to the competitive advantage of fungi under conditions of decreasing water potential and poorer substrate availability.
Compounds that are not further degradable, such as lignin-humus complexes, are formed and become predominant. Some authors have proposed a fifth composting phase, known as the curing phase (or storage phase), during which the physico-chemical parameters do not change, but changes in microbial communities still occur [32].
Therefore, the chemical and microbial changes that the substrate undergoes during the different phases of the composting process will largely determine the stability and degree of maturity of the end product and in turn, its safe use as an organic amendment. Evaluation of compost stability and maturityThe stability and maturity of compost is essential for its successful application, particularly for composts used in high value horticultural crops [33].
Both terms are usually used interchangeably to describe the degree of decomposition and transformation of the organic matter in compost [34], despite the fact that they describe different properties of the composting substrate. Stability is strongly related to the degree to which composts have been decomposed to more stable organic materials [35]. Unstable compost, in contrast, contains a high proportion of biodegradable matter that may sustain a high microbial activity [36].
On the other hand, compost maturity generally refers to the degree of decomposition of phytotoxic organic substances produced during the active composting stage and to the absence of pathogens and viable weed seeds [37]. For instance, physical parameters including temperature, odor and color constitute a very simple and rapid method for stability evaluation, giving a general idea of the decomposition stage reached; however, little information is achieved as regards to the degree of maturation.
In addition, chemical parameters including pH, electrical conductivity, cation exchange capacity (CEC), the ratios of C to N and NH4+ to NO3- and humification parameters have also been widely used as indicators of stability [39]. Nevertheless, several drawbacks have been found regarding these parameters, thereby preventing their use as accurate indicators. In fact, when wastes rich in nitrogen are used as the source material for composting, like sewage sludges or manures, the C to N ratio can be within the values of a stable compost even though it may still be unstable. The increase in CEC with composting time is related to the formation of carboxyl and phenolic functional groups during the humification processes; however, the wide variation in CEC values among the initial substrates prevent to establish a threshold level and to use it as a stability indicator [41]. The principle of the respirometric tests is that unstable compost has a strong demand for O2 and high CO2 production rates as a consequence of the intensive microbial development due to the presence of easily biodegradable compounds in the raw material. Then, as composting proceeds, the decrease in the amount of degradable organic matter is accompanied by a decline in both O2 and CO2 respirometry. The Solvita test, which measures CO2 evolution and ammonia emissions simultaneously have been found to be a simple and easily used procedure for quantifying soil microbial activity in comparison with both titration and infrared gas analysis [42]; this test has also been used for determining the stability degree in diverse composts [43]. Enzymatic activities have also been found suitable as indicators of the state and evolution of the organic matter during composting, as they are implicated in the biological and biochemical processes through which the initial organic substrates are transformed (Tiquia, 2005). These latter authors established that the formation of a stable enzymatic complex, either in moist or air-dried compost samples, could represent a useful index of stabilisation.
Additionally, enzymatic activities, especially dehydrogenases, are considered easy, quick and cheap stability measurements [36]; however, the wide range of organic substrates involved in the composting process makes it difficult to establish general threshold values for these parameters. The hydrolysis of fluorescein diacetate (FDA), which is a colourless fluorescein conjugated that is hydrolyzed by both free (exoenzymes) and membrane bound enzymes [45], has been suggested as a valid parameter for measuring the degree of biological stability of the composting material, as it showed a good correlation with other important stability indexes [46]. The analysis of phospholipid fatty acid (PLFA) composition has also been proposed for determining compost stability [47-48].
These authors found a positive correlation between the proportion of PLFA biomarkers for Gram-positive bacteria and the germination index during the maturation of composting of poultry manure and cattle manure, respectively.
The strength of this lipid-based approach, as compared to other microbial community assays, is that PLFAs are rapidly synthesized during microbial growth and quickly degraded upon microbial death and they are not found in storage molecules, thereby providing an accurate ‘fingerprint’ of the current living community [49]. The potential ability of the microbial community to utilise select carbon sources by determining the community-level physiological profiles (CLPPs) with the Biolog® Ecoplate has also been considered for compost stability testing [50]. The principle is that compost extracts are inoculated onto microtiter plates that contain 31 different C substrates [51-52]. For example, as in reference [32] the authors used three different cultivation-independent techniques based on 16S rRNA gene sequences, i.e. PCR-denaturing gradient gel electrophoresis (DGGE), clone libraries, and an oligonucleotide microarray (COMPOCHIP), in order to evaluate the dynamics of microbial communities during the compost-curing phase.
Influence of compost amendments on the soil microbiotaComposted materials have gained a wide acceptance as organic amendments in sustainable agriculture, as they have been shown to provide numerous benefits whereby they increase soil organic matter levels, improve soil physical properties (increased porosity and aggregate stability and reduced bulk density) and modify soil microbial communities [56]. Substantial evidence indicates that the use of compost amendments typically promotes an increase in soil microbial biomass and activity, as reviewed in [56-57].
This enhancing effect may be attributed to the input of microbial biomass as part of the amendments [58]; however, the quantity of organic matter applied with the compost is very small in comparison with the total organic matter present in the soil and, in turn it is believed that the major cause is the activation of the indigenous soil microbiota by the supply of C-rich organic compounds contained in the composting materials [58]. Such effects on microbial communities were reported to be dependent on the feedstocks used in the process [59]. However, other authors did not find significant differences between soil plots that had been amended with four different compost types (green manure compost, organic waste compost, manure compost and sewage sludge compost) over 15 years [60]. This fact suggests that the soil itself influences the community diversity more strongly than the compost treatments.
Furthermore, C addition to soil seems to select for specific microbial groups that feed primarily on organic compounds. Therefore, it can be expected that the addition of organic amendments not only increases the size of the microbial community but also changes its composition, as has already been observed in previous experiments [61-63]. As shown by [62] higher amounts of composts resulted in a more pronounced and faster effect in the structure of microbial communities, as revealed by PLFA analysis, indicating that the compost application rate is a major factor regarding the impact of compost amendments on soil microbiota.
However, in contrast to fungi, the bacterial community structure, both on the universal and the Streptomycetes group-specific level, were influenced by compost amendments, especially the combined compost and mineral fertilisers treatments. This seems reasonable, as bacteria have a much shorter turnover time than fungi and can react faster to the environmental changes in soil. CLPP profiles have also been used to evaluate the impact of compost amendments on the potential functional diversity of soil microbiota, as they are considered suitable indicators for detecting soil management changes [65].
As shown by [66] different types of compost (household solid waste compost and manure compost) affected differently the substrate utilization patterns of the soil microbial community relative to unamended control soils. Other authors also reported that the sampling date had more weight on CLPP results than compost treatments [63,67]. All these studies together highlight the importance of a multi-parameter approach for determining the influence of compost amendments on the soil microbiota, which is of utmost importance to understand the disease suppressive activity of compost and the mechanisms involved in such suppression [68]. Since the 1980s a large number of experiments have been addressed describing a wide array of pathosystems and composts from a broad variety of raw materials. Interestingly, Noble and Coventry [69] evaluated the suppression of soilborne plant pathogens by compost in both laboratory and field scale experiments.
In general, they found that the effects in the field were smaller and more variable than those observed at lab-scale.
They highlighted that the different composts did not affect the pathogens in the same way and that no single compost was found to be effective against all the pathogens.
Furthermore, in a study carried out with 100 composts produced from various substrates under various process conditions, it was found that those composts that had undergone some anaerobic phase showed the best results in terms of suppressing plant disease [71].
However, up to now, there is still a general lack of understanding concerning the suppressivity of compost [68], as it depends on a complex range of abiotic and biotic factors. The first three affect the pathogen directly and reduce its survival, whilst the latter one acts indirectly via the plant and affect the disease cycle. Whilst, for Rhizoctonia solani, few microorganisms present in compost are able to eradicate this pathogen and, in turn this type of suppression is referred as “specific suppression”.
Overall, all of the above reinforces that the activity of microbial communities in composts is a major factor affecting the suppression of soilborne plant pathogens. Indeed, the disease suppressive effect is usually lost following compost sterilization or pasteurization [68].
Better understanding of the microbial behaviour and structure of the antagonistic populations in the compost will provide tools to reduce its variability.
Actinobacteria were dominant during the mid-curing stage, and no bacterial pathogens were detected even after a year of curing. The addition of antagonistic microorganisms to compost is also a promising technique to improve its suppressivity.
They found that not only the addition of the antagonist is important, but also the strategy of inoculation of the antagonist in order to efficiently colonize the substrate, as the autochthonous microbial community can inhibit it. Ultimately, predicting disease suppression on the basis of pure compost is expected to be highly advantageous for compost producers.

This would enable them to optimise the composting process based on the specific disease jeopardising the target crop. The vermicomposting processVermicomposting is defined as a bio-oxidative process in which detritivore earthworms interact intensively with microorganisms and other fauna within the decomposer community, accelerating the stabilization of organic matter and greatly modifying its physical and biochemical properties [75].
The earthworm species Eisenia andrei, Eisenia fetida, Perionyx excavatus and Eudrilus eugeniae display all these characteristics and they have been extensively used in vermicomposting facilities.Vermicomposting systems sustain a complex food web that results in the recycling of organic matter and release of nutrients [77]. The biochemical decomposition of organic matter is primarily accomplished by the microbes, but earthworms are crucial drivers of the process as they may affect microbial decomposer activity by grazing directly on microorganisms [78-79], and by increasing the surface area available for microbial attack after the comminution of organic matter [8].
Furthermore, earthworms are known to excrete large amounts of casts, which are difficult to separate from the ingested substrate [8]. The contact between worm-worked and unworked material may thus affect the decomposition rates [80], due to the presence of microbial communities in earthworm casts different from those contained in the material prior to ingestion [81].
In addition, the nutrient content of the egested materials differ from that in the ingested material [82], which may enable better exploitation of resources, because of the presence of a pool of readily assimilable compounds in the earthworm casts.
Therefore, the decaying organic matter in vermicomposting systems is a spatially and temporally heterogeneous matrix of organic resources with contrasting qualities that result from the different rates of degradation that occur during decomposition [83]. Specific microbial groups respond differently to the gut environment [84] and selective effects on the presence and abundance of microorganisms during the passage of organic material through the gut of these earthworm species have been observed. For instance, some bacteria are activated during the passage through the gut, whereas others remain unaffected and others are digested in the intestinal tract and thus decrease in number [78]. These findings are in accordance with a recent work that provides strong evidence for a bottleneck effect caused by worm digestion (E. This points to the earthworm gut as a major shaper of microbial communities, acting as a selective filter for microorganisms contained in the substrate, thereby favouring the existence of a microbial community specialised in metabolising compounds produced or released by the earthworms, in the egested materials. Such selective effects on microbial communities as a result of gut transit may alter the decomposition pathways during vermicomposting, probably by modifying the composition of the microbial communities involved in decomposition, as microbes from the gut are then released in faecal material where they continue to decompose egested organic matter. Indeed, as mentioned before, earthworm casts contain different microbial populations to those in the parent material, and as such it is expected that the inoculum of those communities in fresh organic matter promotes modifications similar to those found when earthworms are present, altering microbial community levels of activity and modifying the functional diversity of microbial populations in vermicomposting systems [80].
Previous studies have already shown that a higher microbial diversity exists in vermicompost relative to the initial substrate [19,85].
Upon completion of GAPs, the resultant earthworm casts undergo cast- associated processes (CAPs), which are more closely related to ageing processes, the presence of unworked material and to physical modification of the egested material (weeks to months; Figure 1). During these processes the effects of earthworms are mainly indirect and derived from the GAPs [17].
The length of the maturation phase is not fixed, and depends on the efficiency with which the active phase of the process takes place, which in turn is determined by the species and density of earthworms, and the rate at which the residue is applied [8].
During this aging, vermicompost is expected to reach an optimum in terms of its nutrient content and pathogenic load, thereby promoting plant growth and suppressing plant diseases [8]. However, unlike composting, vermicomposting is a mesophilic process (<35 °C), and as such substrates do not undergo thermal stabilisation that eliminates pathogens.
Nevertheless, it has been shown that vermicomposting may reduce the levels of different pathogens such as Escherichia coli, Salmonella enteritidis, total and faecal coliforms, helminth ova and human viruses in different types of waste [75].
In a recent work [78], a reduction by 98% in the number of faecal coliforms of pig slurry was detected after two weeks of processing in the presence of E. This was consistent with the fact that specific microbial groups respond differently to the gut environment, depending on the earthworm species.
The pathogen considered is another important factor controlling the reduction in the pathogenic load during the process. In a recent study [89] a decrease in the abundance of faecal enterococci, faecal coliforms and Escherichia coli was recorded across the layers of an industrial-scale vermireactor fed with cow manure; whereas no changes were reported for total coliforms, Enterobacteria or Clostridium.
These findings are of great importance for the optimisation of the vermicomposting process because despite the pioneering studies of Riggle [90] and Eastman et al. This selective effect on pathogens indicates that earthworms not only modify the abundance of such pathogenic bacteria but also alter their specific composition.
According to [89], the unaffected pathogens could benefit as a result of the overall decrease in bacterial and fungal biomass across the layers of the reactor, thereby diminishing possible competition for resources.Collectively, the aforementioned studies highlight the importance of monitoring the changes in microbial communities during vermicomposting, because if the earthworms were to stimulate or depress microbiota or modify the structure and activity of microbial communities, they would have different effects on the decomposition rate of organic matter, thereby influencing the vermicompost properties, which is critical to guarantee a safe use of this end-product as an organic amendment and thus benefit both agriculture and the environment.
Thus, earthworm activity is expected to have a greater effect on bacteria than on fungi in these organic substrates in the short-term [79].
In line with this, a significant increase in the fungal biomass of pig manure, measured as ergosterol content, was detected in a short-term experiment (72 h) with the earthworm species E.
A higher fungal biomass was found at intermediate and high densities of earthworms (50 and 100 earthworms per mesocosm, respectively), which suggests that there may be a threshold density of earthworms at which fungal growth is triggered.
This priming effect on fungal populations was also observed in previous short-term experiments in the presence of the epigeic earthworms Eudrilus eugeniae and Lumbricus rubellus fed with pig and horse manure, respectively [16,86]. These contrasting short-term effects on bacterial and fungal populations are thus expected to have important implications on decomposition pathways during vermicomposting because important differences exist between both microbial decomposers related to resources requirements and exploitation [92]. This is based on the fact that fungi can immobilise great quantities of nutrients in their hyphal networks, whereas bacteria are more competitive in the use of readily decomposable compounds and have a more exploitative nutrient use strategy by rapidly using newly produced labile substrates [92]. The above-mentioned studies dealing with the effects of epigeic earthworms on microorganisms have focused on the changes before and after the active phase rather than those that occur throughout the whole vermicomposting process. Hence, in a current research study, and using a continuous-feeding vermicomposting system, we evaluated the different phases of interaction between earthworms and microorganisms and additionally, we monitored the stabilisation of the fresh manure during a period of 250 days.
At the end of the experiment we obtained a profile of layers of increasing age, resembling a time profile, with a gradient of fresh-to-processed manure from the top to the bottom. This type of system allowed us to evaluate whether and when the samples reached an optimum value to be classified as vermicompost, as regards to the stabilisation of organic matter and the levels of microbial biomass and activity. Briefly, we used polyethylene reactors (n=5) with a volume of 1 m3, which were initially comprised of a 10 cm layer of mature vermicompost (a stabilised non- toxic substrate that serves as a bed for earthworms), on which earthworms (Eisenia fetida) were placed and a layer containing 5 kg of fresh rabbit manure, which was placed over a plastic mesh (5 mm pore size) to avoid sampling the earthworm bedding. New layers with the same amount of fresh manure were added to the vermireactor every fifty days according to the feeding activity of the earthworm population. The reactors were divided into 4 quadrants and two samples were taken at random from each quadrant with a cylindrical corer (8 cm diameter). Each corer sample was divided into five layers of increasing age and the samples from the same layer and each reactor were gently mixed to analyse the changes in microbial communities. The structure of the microbial communities was assessed by PLFA analysis; some specific PLFAs were used as biomarkers to determine the presence and abundance of specific microbial groups [93].
Total microbial activity was also assessed by measuring the rate of evolution of CO2, as modified for [17] for samples with a high organic matter content. Thus, the upper layers (50 and 100 days old) along with the fresh manure were clearly distinguished from the intermediate (150 days old) and lower layers (200 and 250 days old) (Figure 2).
Figure 2.Changes in the microbial community structure throughout the process of vermicomposting assessed by the principal component analysis of the twenty-seven PLFAs identified in the layers of reactors fed with rabbit manure.
These results are in accordance with previous studies based on PLFA profiles, with marked changes in the structure of microbial communities due to decreases in both bacterial and fungal populations throughout the process of vermicomposting [18, 89]. Accordingly, a reduction in the dissolved organic carbon content was detected from upper to lower layers (Figure 4B), reaching a value close to 7000 µg g-1 dw after 250 d of vermicomposting. In contrast, other authors [17] reported levels of DOC much more lower in a long-term experiment (252 days) with the epigeic earthworm E.
Values are means ± SE.Overall, in the present study a higher degree of stabilisation was reached in the rabbit manure after a period of between 200 and 250 days, as indicated by the lower values of microbial biomass and activity that are indicative of stabilized materials. These results underscore the potential of epigeic earthworms in the stabilisation of this type of organic substrates, which is of great importance for the application of animal manures as organic amendments into agricultural soils because, as already mentioned, it is widely recognised that the overproduction of this type of substrate has led to inappropriate disposal practices, which may result in severe risks to the environment [6]. Influence of vermicompost amendments on the soil microbiotaAs occurred with compost amendments, vermicompost has also been found to provide manifold benefits when used as a total or partial substitute for mineral fertiliser in peat-based artificial greenhouse potting media and as a soil amendment in field studies [95].
Among the advantages of vermicompost as a soil amendment is its potential to maintain soil organic matter, foster nutrient availability, suppress plant diseases and increase soil microbial abundance and activity.
Despite these limitations, some recent findings have been made, thereby contributing to better understand whether and to what extent vermicompost amendments affect soil microbial biomass, activity and community structure.
Increases in the microbial activity and in the activity of the soil enzymes involved in the release of the main plant macronutrients with vermicompost amendments, have also been signalled in several studies [96-98].
Such increase could be due to the fact that soil microorganisms degrade organic matter through the production of a variety of extracellular enzymes and, in turn an input of organic matter is expected to be accompanied by a higher enzymatic activity.
Moreover, the added material may contain intra- and extracellular enzymes and may also stimulate microbial activity in the soil [99]. Additionally, vermicompost has been found to promote the establishment of a specific microbial community in the rhizosphere different from that of plants supplemented with mineral fertilisers or other types of organic fertilisers such as manure [100]. Inorganic fertilisation only supplies N, P and K, whereas organic fertilisers also supply different amounts of C and macro- and micronutrients, which can select for microbial communities with different nutritional requirements [95].
Moreover, microbial communities in vermicompost are metabolically more diverse than those in manure [17], and may be incorporated, at least in the short-term, to soils [101]. They found differences in the bacterial community structure between the different amendments and these differences persisted for at least one month after seedlings were transplanted to the field. Since both compost and vermicompost were made from the same parent material, such differences could be due to the way in which the organic matter was processed prior to the amendment [102]. Previous comparisons between vermicompost and compost with respect to microbial communities [103-105] are difficult to interpret because different feedstocks were used for each process. Compost feedstocks are known to alter the material’s effects on the structure of the microbial communities [86], so it is essential to use composts made from the same feedstock in order to draw valid comparisons between the two biological processes.
Furthermore, it may be expected that different hybrids or plant genotypes will respond differently to vermicompost, considering that plant genotype determines important differences in nutrient uptake capacity, nutrient use efficiency and resource allocation within the plant.
Different genotypes may therefore enhance root growth or modify root exudation patterns in order to increase nutrient uptake [100], and all of these strategies will determine the establishment of different interactions with the microbial communities at the rhizosphere level. Indeed, disease suppressiveness is obviously linked to the microbiota added with the vermicompost, along with the biological and physicochemical characteristics of the native soil microbial community.
However, despite the large body of scientific evidence showing the positive effects of vermicompost regarding the suppression of soil-borne plant fungal diseases (reviewed in [75,108]), it is still necessary to obtain a deeper understanding of the mechanisms involved and the main factors influencing such suppressing effects. According to the mechanisms proposed for compost [68-69], disease suppression by vermicompost may be attributed to either direct effects or to the induction of systemic resistance in the plant. Some of the indirect effects of vermicompost have been related to changes in the microbiological properties of the soil or the potting media. Processing by earthworms during vermicomposting has a strong effect on the microbial community structure and activity of the initial waste [8].

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