1. Introduction
The concept of using fly larvae for processing organic waste was initially proposed almost 100 years ago [
1]. More recently, the black soldier fly (BSF), which is raised on animal manure or household organic waste (HOW) as feed for livestock, is being considered as an efficient way to recycle unutilized resources in a sustainable manner [
2]. However, due to restrictions from sanitary laws and a lack of public acceptance for processing HOW for this purpose [
3], several companies currently raise BSF larvae on cereal byproducts. Subsequently, the BSF larvae meal is sold as feed for animals [
4] and BSF larvae production residue (BSFR) is sold for fertilizer.
Although using only cereal byproducts for BSF larvae production will maintain the safety of feed for livestock, this regulation may inhibit the possibility of sustainable resource recycling technology. The BSFR could be used as an organic fertilizer because BSF larvae can use livestock manure and HOW as a food source [
5,
6], which is typically disposed of as organic waste [
6]. However, most previous studies on BSF larvae production have been conducted to develop efficient organic waste treatment conditions for BSF larvae production.
A previous study on the density of BSF larvae reported that a larval density of 1.2 larvae/cm
2 and a feeding rate of 163 mg/larva/day (dry base) were optimal for ideal organic waste disposal [
7]. Although, in the case of one feeding, the individual larvae weight was more affected by the nutrient concentration of the feed than the density of larvae [
8].
Efficient BSF larvae production methods are currently being investigated; however, very few studies currently exist on the fertilizer value of BSFR made from HOW. In a recent study, a mixture of municipal solid organic waste from factories and households was treated with BSF larvae [
6]. This study reported that the heavy metal content in municipal solid organic waste was reduced and the heavy metal content in the residue was below the threshold for fertilizer use [
6]. However, the study did not investigate microorganisms in the residue and evaluate its effects on plants. Therefore, a detailed evaluation of the HOW-derived BSFR has still not been conducted. Although some microbial benefits of BSF larvae production have been reported, in particular a reduction in
Escherichia coli in livestock manure [
9,
10], it appears that only one study has investigated the microbiota of BSFR [
11]. Furthermore, to date no detailed studies that analyzed the fertilizer value of BSFR exist. Thus, this present study aimed to better explain the nutrient composition and suitability of BSFR as a fertilizer in comparison with commercial compost.
4. Discussion
The final chemical composition of BSFR differed from EHOW and other commercial composts, and was distanced from the other groups in the PCA plots. BSFR had a higher N and ash in its chemical composition compared to EHOW because BSFR includes larval feces and molted residues. Moreover, P and K were slightly lower which is possibly due to their use for larval growth. Since BSFR was produced only by larval processing and air-drying, its final composition was similar to poultry manure composts. However, the concentration of NO
3-N in the poultry manure was higher than NH
4+-N because it had been processed through the animal, deposited, and subsequently dried. Conversely, BSFR showed a higher concentration of NH
4+-N than NO
3-N, which is likely as BSFR was only treated by larvae and did not experience the microbial fermentation process associated with animal digestion and deposition. Previous reports indicate that the application of fertilizers and manures derived from livestock excrement containing high levels of NO
3-N have led to the accumulation of NO
3-N in vegetables and drinking water, resulting in health risks [
19]. However, BSFR, unlike conventional livestock manures, may be a new fertilizer with less concern of potential NO
3-N accumulation. Moreover, since higher cation exchange capacity (CEC) soil can retain ammonium ions in the soil colloids [
20,
21], BSFR may be suitable in higher CEC soil. However, NH
4+-N can volatilize as ammonia when it comes into contact with the alkaline soil, and volatilize as nitrite gas when it comes into contact with acidic soil [
20,
21,
22]. This gas can cause injury to plants (e.g., tomato, green pepper, or eggplant) [
23,
24]. Hence, the application method for BSFR would be a future concern.
In the PCA, a positive correlation was observed among the analyzed properties excluding moisture, C, C/N ratio, and EC in PC 1. Thus, PC 1 could be considered in the evaluation of the main fertilizer nutrients for plants, such as N, P, and K. Moreover, a positive correlation was also recorded for pH, which is acidic in the early stages of composting due to organic acids, but gradually mineralizes and becomes alkaline [
25,
26]. This might indicate that the concentration of fertilizer nutrient compositions in the samples increased as the PC value increased positively, and the pH tended to be alkaline. Whereas, the negative values were larger in the samples with a higher C/N ratio due to the abundance of organic matter. In general, organic wastes have high moisture and high organic matter, and if they are applied as fertilizer without fermentation by composting, the germination of plants will be inhibited and their growth will be damaged [
27]. Thus, higher negative PC values would indicate that the sample is close to the unfermented condition and does not sufficiently work as a fertilizer. In PC 2, negative correlations were found for TN, P, and EC, while positive correlations were found for C/N ratio, Cu, and Fe. These results indicate that for PC 2, when the value of the PC increased negatively, the sample was rich in TN and P, and the EC value was also high; when the value of the PC increased positively, the C/N ratio was high and the Cu and Fe content were high. In PC 3, there was a positive correlation with ammonium nitrogen, which suggests that the concentration of NH
4+-N was higher when the PC value was positively increased. In PC 4, each sample plotted in approximately the same position, a situation that also makes it difficult to characterize the other PC. PC 1 represents the compost characteristics of each sample, and PCs 2 and 3 represent the detailed compost characteristics that support PC 1.
The livestock manures are plotted at different locations in the plots of PC 1 and 2 due to their corresponding characteristics. Despite this, they are considered ready for use as fertilizer. The plots demonstrated that EHOW was plotted at a farther distance from the livestock manures and is not ready for use as a fertilizer in its original condition. Although BSFR is closer to livestock manures than EHOW, it had high moisture and a high EC value for the conditions used in this study. Therefore, BSFR can be better processed for fertilizer use by increasing the period of larval processing, drying, and reducing the organic matter.
The top 10 microbiota for BSFR in terms of relative abundance were similar to those in poultry, but the structure of BSFR demonstrated a distinct composition. Unlike poultry manure, BSFR is not subject to composting for a long period of time, which was evident from its chemical composition. This may occur because BSFR is a dry product of animal feces.
Sporosarcina, which exhibited a high abundance of BSFR microbiota was also detected in the BSF larvae and the feed residue [
11]. Hence, this suggests that
Sporosarcina originated from larvae. In the α diversity, BSFR did not show any significant differences with other commercial composts, indicating that the diversity of constituent bacteria was similar to commercial composts. In the β diversity, BSFR plotted at far distances from EHOW, which suggests that changes in the constituent bacteria were caused by larval processing. Moreover, although BSFR plotted near horse, it was plotted closest to poultry, indicating that the microbiota of BSFR was closest to that of poultry manure, similar to the results of the top 10 bacterial composition.
It is important to determine whether BSFR is safe for plant and human health when considering its use as a fertilizer. The abundance of
Escherichia in EHOW was reduced by larval processing, which confirms that BSFR can be used as a fertilizer, in addition to a commercial compost. However, caution should be taken in the application of BSFR as a fertilizer for vegetables of Brassicaceae, vineyards, or citrus orchards, as Xanthomonadaceae was recorded in high abundance in the microbiota of BSFR. This family includes two genera
Xanthomonas and
Xylella which can cause disease in plants [
28,
29,
30,
31].
In the Komatsuna cultivation test, there was no difference in the germination rate for standard condition A when fertilizer was applied to a starting total of 100 mg of total nitrogen per pot. Although BSFR contains Xanthomonadaceae, which includes a potentially disease-causing bacteria, no pathogens were observed in the Komatsuna during the cultivation test and they appeared to grow normally. Moreover, under condition A, the highest values for the fresh and dry weights of the Komatsuna were from BSFR. Hence, BSFR can be applied as a commercial fertilizer if the amount of nitrogen is adjusted to standard application levels. The conversion of organic waste into BSFR by BSF larvae is better than using organic waste as fertilizer directly as the germination rates of EHOW and the BSFR Komatsuna were almost the same under condition B. However, the fresh and dry weights for the day 21 EHOW and BSFR Komatsuna were more than twice as high in the initial BSFR group. The common fertilizer values (nitrogen, phosphorus, and potassium) and the values of other chemical compositions that were altered by larval processing may have affected Komatsuna growth. This is strongly suggested by the weakly acidic pH that is suitable for growing plants but was only recorded in EHOW [
16], as well as the fresh weight which was the lowest of all groups. Therefore, rather than directly using the organic waste as a fertilizer it is beneficial in plant production to use organic waste as feed for BSF larvae and then use the residue as fertilizer. Under the conditions of the present study, it is evident that if BSFR is applied at 1/20 of the amount of soil, then there is no yellowing of leaves due to nitrogen deficiency, which was observed in the horse group. This result was also apparent when BSFR was applied at 1/30 of the amount of soil. The germination of Komatsuna was inhibited when 1/10 of the amount of BSFR was applied to the soil. These results indicate that applying such a large amount of BSFR to the soil is not recommended. This recommendation is further reinforced as BSFR recorded the highest EC value.