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Providing hygienic, affordable and manageable sanitation is vital to the improvement in public health in both developed and developing countries. 2.6 billion people in developing regions have no access to improved sanitation (WHO/UNICEF 2010). With 44% of these people practicing open defecation, there are serious risks to public health that can lead to an increase in disease spread (Esrey et al. 1991). Strong evidence suggests that improved sanitation has a significant effect on health in developing regions (Esrey et al. 1991).
On-site improved sanitation includes pit latrines with slabs, ventilated improved pit latrines (VIP), pour-flush pit latrines and composting toilets (WHO/UNICEF 2010). 1.7 billion people in low- and middle-income communities around the world use these forms of improved sanitation (WHO/UNICEF 2010). However, it has been reported in Vietnam (Biran 2010a) and Tanzania (Biran 2010b) that the biggest problem faced by pit latrine owners is the disposal of pit latrine waste. Adequate pit latrine emptying services are not available in many areas in developing countries and can be expensive (Still 2002). The emptying process can also be inconvenient for the latrine owner and cause bad smells in the surrounding area (Biran 2010a,b). Digging a new pit is an alternative, but too expensive for many. Also, it may be impossible in areas which lack space, such as emergency camps and unplanned settlements (Patinet 2010).
Effective treatment and management of human faecal waste is vital to prevent adverse health and environmental effects (WHO/UNEP 2006). The method of waste treatment must be considered, particularly in low-income countries with insufficient piped sewerage systems. It is possible to remove pathogens while transporting faecal sludge to a wastewater treatment plant, but in practice, unregulated services and the prohibitive cost, lack of infrastructure and resources render this method of waste treatment in developing countries unfeasible (Helmer & Hespanhol 1997; Kariuki et al. 2003; WHO/UNEP 2006). Composting can be used to remove pathogens in sewage sludge if maintained correctly (USEPA 2003). But pathogens are not always inactivated throughout the entire compost mass (Droffner & Brinton 1995; Hutchison et al. 2005). Biogas systems combine human excreta with animal waste, agricultural waste and water (NNFCC 2011), but only remove some of the pathogenic organisms. With a large increase in the number of pit latrines being built in developing countries, more consideration needs to be given to improving methods of pit emptying and safe waste processing and disposal.
One prospective solution for waste processing is the larvae of Hermetia illucens (L.), commonly known as the black soldier fly larvae (BSFL). The adult flies are neither a nuisance species nor a mechanical vector of disease, as they do not need to feed, surviving on fat stores from their larval stage (Furman et al. 1959). As the females oviposit around the edges of larval food sources (Copello 1926), they do not transmit pathogens from faecal waste to human food unlike filth flies such as Musca domestica. Although there have been rare cases of accidental myiasis caused by the consumption of ripe, unwashed fruit (Calderón-Arguedas et al. 2005; Fuentes Gonzalez & Risco Oliva 2009), but given their worldwide distribution (Leclercq 1969), such cases represent negligent risks to humans. Unlike the adults, the larvae are detritivores feeding on human cadavers (Dunn 1916), decaying vegetables (Malloch 1917), human pit latrine waste (Bradley 1930) and animal manure (Tingle et al. 1975; Booram et al. 1977; Newton et al. 2005). The final larval stage (prepupal) is indicated by a change in colour from white to dark brown (May 1961). The prepupae crawl out of the feeding material to pupate, climbing slopes of 40° when dry, making them easy to direct for harvesting (Sheppard et al. 1994). The prepupal stage contains high protein and fat levels, 42–45% and 31–35%, respectively (Hale 1973; Newton et al. 1977). These nutritional qualities give the prepupae value, as they can be converted into beneficial end products (Sheppard et al. 1994). They can provide a suitable replacement for conventional fat and protein sources and can be fed to animals such as cockerels (Hale 1973), pigs (Newton et al. 1977), catfish and tilapia (Bondari & Sheppard 1987), and rainbow trout (St-Hilaire et al. 2007). The prepupae can also be fractionated into their component parts; protein separated for animal feeds and fats converted into biodiesel (Li et al. 2011a,b). BSFL are also known to reduce oviposition of the disease-spreading house fly, M. domestica (Sheppard 1983). The quantities of organic material consumed by BSFL can significantly reduce swine, chicken and cattle manure in the animal husbandry industry (Sheppard et al. 1994; Newton et al. 2005). BSFL can also reduce Escherichia coli and Salmonella enterica pathogen loads in chicken and cattle manure (Erickson et al. 2004; Liu et al. 2008), and human faeces (Lalander et al. 2013).
Although there has been much research focusing on the use of BSFL to manage swine, chicken and cattle manure (Sheppard et al. 1994; Newton et al. 2005), as well as municipal organic waste (Diener et al. 2009, 2011), few studies investigated their consumption of human faecal waste (Dang 2010; Lalander et al. 2013). This study aims to determine the efficiency of BSFL at consuming fresh human faeces, under different feeding conditions and feeding rates. Efficiency is determined by calculating waste reduction, bioconversion and feed conversion rates (FCR). The results will help optimise the way in which BSFL are fed human faeces, increasing waste reduction and prepupal biomass generation. The value of the various components of the prepupae could provide a source of income; the economic benefits through selling BSF products could be an incentive to communities, entrepreneurs, non-government organisations and governments to improve faecal sludge management.
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The BSFL fed fresh faeces every 2 days developed into smaller prepupae (Table 3) faster than the larvae fed once at the beginning of the experiment (Figure 1). Based on the slower development and larger prepupae of the larvae fed once, it is theorised that there was a nutritional imbalance in the lump amount diet that led to an increase in consumption to compensate for deficient nutrients (Raubenheimer & Simpson 1997; Bennett 2000; Wright et al. 2003). Both proteins and carbohydrates are critical in the development of insect larvae (Bennett 2000; Nijhout 2003; Lee et al. 2004; Simpson et al. 2006). However, there are few data regarding the protein and carbohydrate content of fresh and ageing faeces. If pit latrine material is used as a proxy, with the top layer being fresh material, and lower layers aged material, the protein content of the material drops rapidly within the first 20 cm (J. H. J. Ensink & B. Torondel, unpublished data). The increase in development time and larval size supports the hypothesis that reduced protein content in the lump sum diet causes a nutritional imbalance that leads to compensatory feeding. If the ageing material is losing nutritional value over time, and the feeding rate of insect larvae is highest in the later instars, it is likely that the older larvae will need to consume more low nutrition feed than larvae fed fresh, nutritionally balanced feed.
Growth rate plasticity (Metcalfe & Monaghan 2001; Tu & Tatar 2003; Wright et al. 2003; Dmitriew & Rowe 2005; Dmitriew 2011) means that larvae are capable of successfully developing on a range of resources that may be transient in nature. Insect herbivores are known to increase their consumption of plant tissue when feeding on low-quality plants (Kondoh & Williams 2001), which increases developmental time and leads to higher vulnerability to natural predators. A slow-growth, high-mortality hypothesis has been proposed in Lepidoptera (Benrey & Denno 1997; Fordyce & Shapiro 2003; Medina et al. 2005; Cornellisen & Stiling 2006) and Coleoptera (Häggström & Larsson 1995). Growth rate plasticity indicates that BSFL could be capable of consuming pit material with a range of nutritional contents and still be capable of developing into valuable prepupae.
Waste reduction, prepupal yield and feed conversion rates
The results from this study were calculated using wet weight, meaning results can only be compared to studies that calculate wet weight waste reduction. It can be seen that waste reduction levels in Groups B and C are comparable (Table 5) to those found when BSFL feed on chicken manure (Sheppard et al. 1994). It is possible that dry weight waste reduction could compare to that found with BSFL feeding on municipal waste (Diener et al. 2011); however, those data were not collected in this experiment. The waste reduction in Group A was far lower; however, this is to be expected with only one larva present for each replicate.
Table 5. Effect of different feed sources on Hermetia illucens mean (±SE) prepupal weight, waste reduction capacity, prepupal yield, bioconversion and feed conversion rate (FCR). The most efficient bioconversion and FCR results are in bold. Other data are from previous studies into swine manure (Newton et al. 2005), chicken manure (Sheppard et al. 1994) and municipal organic waste (Diener et al. 2011)
|Feed source|| ||Mean Prepupal weight (g)||Feed added||Residue||Feed consumed||Waste reduction, %||Prepupal yield||Bioconversion (%)||FCR|
|Swine manurea|| ||N/A||68 kg||42 kg||26 kg||≈ 39||≈ 2.7 kg||3.97||9.6|
|Chicken manureb|| ||0.220 ± N/A||5240 kg||≈ 2620 kg||2620 kg||≈ 50||196 kg||3.74||13.4|
|Municipal organic wastea|| ||0.220 ± 0.008||151 kg||48 kg||103 kg||68||17.8 kg||11.78||14.5|
|Group||Feeding regime|| || || || || || || || |
|A||FR-1||0.2258 ± 0.0078||390 g||260 g||130 g||33||8 g||2.1||15.6|
|FR-2||0.3151 ± 0.0124||482 g||360 g||121 g||25||12 g||2.4||10.4|
|B||FR-1||0.1936 ± 0.0026||437 g||220 g||217 g||50||70 g||16.0||3.1|
|FR-2||0.2986 ± 0.0039||483 g||261 g||221 g||46||108 g|| 22.3 || 2.0 |
|C||FR-1||0.1998 ± 0.0034||658 g||301 g||357 g||54||108 g||16.4||3.3|
|FR-2||0.2410 ± 0.0098||721 g||327 g||393 g||55||131 g||18.1||3.0|
The percentage pupation ranged from 82.8 to 92.5% (Table 3), excluding Group C, Feeding Regime 2. The low figures of pupation in this group (8.2%) could be due to competition between the larvae combined with reducing quality of feed. However, a higher rate would have been recorded if the experiment had lasted longer. Therefore, a 90% yield of prepupae was calculated to compare the FCR against previous research (Table 5). The bioconversion and FCR of the single prepupae in Group A were comparable to the rates found in previous studies (Sheppard et al. 1994; Newton et al. 2005; Diener et al. 2011). However, Groups B and C have higher bioconversion rates and lower FCR values than reported in previous studies. The high bioconversion rates show that BSFL are effective at reducing human faeces, and a low FCR indicates that the larvae feeding on the lower feeding ratio of 100 mg/larva/day are more efficient at converting fresh human faeces into biomass than swine manure, chicken manure and municipal organic waste.
Based on a yield of 90% prepupae, the high waste reduction and effective FCR results support the use of BSFL in human waste management. The prepupae can be collected for their protein and fat, taking advantage of their self-harvesting behaviour of crawling out of their feeding medium. This behaviour removes issues that arise from separating them from remaining residue. However, it is unlikely that all of the prepupae will self-harvest, suggesting alternative methods of prepupal collection must be investigated for large-scale waste management solutions. Also, with further research, the waste reduction could be optimised, resulting in less remaining residue.
In summary, the study has demonstrated that BSFL feeding on fresh human faeces can develop successfully. The largest prepupae are produced when given a large quantity of feed, resulting in prepupae of a higher mass than previous studies. The larvae are effective at waste reduction and converting the waste into a valuable biomass. These results support the use of BSFL in a human waste management solution. However, a number of issues still need to be addressed. It has been shown that BSFL are capable of consuming fresh human waste on a small scale. However, upscaling of this experiment is needed to test whether BSFL are capable of developing into prepupae at high densities. To help develop the technology for use in developing countries, more research needs to be conducted on the ability of BSFL to consume pit latrine waste. Previous research shows how BSFL development time varies depending on diet, feeding rate, temperature and humidity (Tomberlin et al. 2002, 2009; Diener et al. 2009, 2011; Holmes et al. 2012). Therefore, further research is needed to assess the growth rate plasticity of BSFL on low-quality diets like pit latrine material. The BSFL will have to be tested on material from different latrine types, with different physical and chemical characteristics recorded to determine effects on waste reduction and prepupal yield. Also, considering that the prepupal biomass could be used to feed animals that are part of the human food chain, it is important to assess the potential risks regarding bioaccumulation of heavy metals and contamination by pathogens.
Ultimately, BSFL have the potential to improve sanitation in developing countries by providing a way to process dangerous human faecal waste, with the benefit of having the prepupae produced have a value that could provide a source of income for communities or local entrepreneurs, while the remaining residue, if safe, may be used as a fertiliser or soil conditioner.