Mass production of maggots for fish feed using naturally occurring adult houseflies (Musca domestica)

Lugano Hezron, Nazael Madalla¹ and Sebastian W Chenyambuga¹

National Service Headquarters, Directorate of Agriculture and Livestock P.O. Box 1694, Dar es Salaam, Tanzania
lhlutengano@gmail.com
¹ Department of Animal, Aquaculture and Range Sciences, Sokoine University of Agriculture P.O. Box 3004, Morogoro, Tanzania

Abstract

Housefly maggots were cultured on various organic wastes viz. cow manure, poultry manure, pig manure, cattle offal and kitchen leftovers, using developed culture units. The suitability of developed culture units and the effects of type of substrate of culture, length of culture and mass of substrate on wet yield and proximate composition of maggots were assessed.

There was significant difference in wet yield between the substrates, the values being 50.5, 40.8, 27.3, 27.2 and 21.6 g/kg for cattle offal, poultry manure, pig manure, kitchen leftovers and cow manure, respectively. Increased length of culture, from 3 to 5 days post oviposition, led to a significant increase in total maggot wet weight (110, 119 and 128 g/kg), fat contents (23.1, 25.4 and 29.3%), crude fibre contents (6.2, 6.4 and 7.2%) and a decline in crude protein contents (48.6, 46.7 and 44.6%) respectively. Similarly, the total maggot wet weight increased by 27% as mass of substrate was doubled from 12 to 24 kg in the culturing chamber. From the study it is concluded that, for optimum wet yields and highest fat content, harvesting maggots 5 days post oviposition is more appropriate whereas, for highest protein content harvesting is desirable on third day of maggot formation. Also 24 kg of wet poultry manure per 1.06 m² culturing bed is optimal for highest total maggot wet yields. Further studies to enable commercial availability of maggot meal with subsequently extensive use in fish nutrition by small scale farmers are recommended.

Key words: length of culture, mass of substrate, proximate composition, wet yield

Introduction

Houseflies (Musca domestica) are the most diverse group of flies, capable of turning decaying organic matters into nutritionally rich food of animal origin (Hussein et al 2017). They are easy to produce and process (Anene et al 2013; Aniebo and Owen 2010), and relatively cheaper than other sources of animal protein (Ajani et al 2004). Maggots can grow on various organic wastes such as pig dung (Pastor et al 2011), cattle blood and wheat bran (Aniebo and Owen 2010), poultry manure (Hwangbo et al 2009), cattle gut and rumen content (Anene et al 2013). The maggots are fairly nutritious with 10.2% moisture, 56.3% crude protein, 22.3% crude fat and relatively high amounts of micronutrients (Anene et al 2013; Hussein et al 2017). Trials to partially or completely replace costly fishmeal in fish diets with the maggot meal have shown promising results (Idowu and Afolayan 2013; Ajani et al 2004; Sogbesan 2014). Ajani et al (2004) reported that replacement of fishmeal up to 100% maggot meal in diets of Nile tilapia ‘Oreochromis niloticus’ improved growth and also led to a reduction in the cost of production by 18 to 28%. However, wide use of maggot meal in aquafeed industry is limited due to unavailability of adequate amounts of maggot meal. The current study is therefore aimed at developing technique for mass production of housefly maggots.

Materials and methods

Study area

This study was conducted in the Aquaculture Research Facility of the Department of Animal, Aquaculture and Range Sciences (DAARS) of Sokoine University of Agriculture (SUA). The University lies at the foot of Uluguru Mountains, at an altitude of about 500 - 600 meters above sea level. The area is situated 6^° S and 37^° E and it is 3 km away from town centre of Morogoro region of Tanzania. The annual rainfall ranges between 600 and 1000 mm per annum and the temperature ranges between 30^°C and 35^°C during the hottest months (October to January) and 20^°C to 27^°C in the coolest months (April to August).

Maggot production system

The system was made of plastic culture units, each consisted two chambers: the top and the bottom (Figure 1). The top chamber of the unit was the maggot culturing chamber (inner dimensions 47 x 37 x 7 cm), and was open at the top for access to houseflies for laying their eggs on the exposed substrate. The base of this chamber was screened with 3 mm galvanized wire mesh net to allow dropping of the maggots. The bottom chamber, with a covered outlet, was the collection chamber (inner dimensions 47 x 37 x 14 cm) where the maggots were collected. During harvesting, the substrate containing maggots was turned up with aid of wooden flat bar under intensive sunlight. In an attempt to escape from traces of sunlight, maggots passed through the 3 mm mesh size net and dropped in the bottom chamber where they were easily collected through the outlet of the collection chamber. All the culture units were placed on a constructed long wooden platform at least 30 cm above the ground. The platform with culture units was set up under shed to avoid direct effect of sunlight.

Figure 1. Cross section of maggot culture unit. 1 - top (culturing) chamber, 2 - a 3 mm galvanized wire mesh net, 3 - bottom (collection) chamber, 4 - maggot collection outlet.

Experimental set up for maggot production

Two trials were carried out. The first trial assessed the suitability of the developed culture units using locally available substrates. Fresh organic substrates namely: cow manure, poultry manure, pig manure, cattle offal and kitchen leftovers were collected from vicinity of the University. Each substrate was placed in air tight container overnight to neutralize any fly eggs or larvae that could be present at the time of collection. A total of 2.5 kg of each of the substrates was mixed with 0.25 kg of fly attractant composed of blood, meat debris and rotten eggs and placed randomly in triplicates in culture units. The units were exposed for eight hours to attract houseflies to naturally lay their eggs (oviposition). The substrates were then covered with perforated black polythene sheet to provide darkness. The substrates were kept moist by sprinkling of water once daily. Harvesting was done after four days where maggots were collected, washed, blanched with hot water and then weighed to obtain total maggot wet weight per substrate.

In the second trial, a selected substrate was used to assess effects of length of culture and mass of substrate on wet yield and proximate composition of maggots. The maggots were cultured in scaled-up units with dimensions of 1 x 0.6 x 0.1 m (Figure 1). Two substrate mass treatments of 12 and 24 kg were tested in triplicates to assess the effect of quantity of substrate on wet maggot yield. The two masses were evenly spread at a thickness of 1.8 and 3.7 cm respectively in the same size culturing chambers. Effect of length of culture was assessed at three days, four days and five days post oviposition. The yields were expressed in g of wet maggots per kg of fresh substrate.

Harvested maggots were oven dried at 70^°C to constant weight and milled through a 1 mm sieve using a 7446 Christy HEL laboratory mill (Christy Hunt Engineering, UK). Milled samples were stored frozen until laboratory analyses were done. Proximate analysis was undertaken according to methods described by Association of Official Analytical Chemists (AOAC 2005). Crude protein was determined using the Kjeldahl method. The amount of nitrogen which was multiplied by factor of 6.25 to get crude protein was determined by digesting samples using 12 1009 digester (Tecator, Sweden) followed by distillation using 2200 Kjeltic Auto-analyzer (Foss Tecator, Sweden). Ether extract was determined using a Soxtec HT 1043 (Tecator, Sweden) and was extracted using petroleum ether, BP 40-60^°C. Crude fibre was determined using a moisture free defatted sample which was digested by weak sulphuric acid followed by a weak sodium hydroxide using the ANKOM 220 system (ANKOM technology, USA). Ash was determined by incineration of sample at 550^°C for 3 hours in a muffle furnace N31R (Nabertherm, West Germany).

Data analysis

Collected data were statistically analyzed using Generalized Linear Model (GLM) at 5% of probability. The means were separated using Tukey’s significant difference test through the statistical program SAS version 8.0 (SAS Institute 2000).

Results

Suitability of culture units

Culture units were developed to serve as appropriate culture technique for production of large volume of housefly maggots with convenient harvesting. In that context, the suitability of the developed culture units in achieving the goal of this study was realized through observation of appreciable quantities of maggots recovered from the substrates (Tables 1, 2 and 4). A number of advantages were also realized with using of developed culture units, including simple design as shown in Figure 1 which does not require any complicated apparatus or additional source of energy other than sunlight to aid separation of the maggots. Thus, harvesting maggots was more convenient as large quantities of maggots were easily collected from the harvest chamber through the collection outlet.

Effect of type of culture substrate on maggot wet yield

Type of substrate had significant effect on yield of maggots as shown in Table 1. Cattle offal gave highest yield followed by poultry manure and least yield was observed in cow manure.

Effect of length of culture on maggot wet yield

Length of culture significantly influenced wet yields of maggots as shown in Table 2. The yield increased with length of culture. Highest wet yield was observed after five days of culture and least after three days of culture.

Effect of length of culture on proximate composition of maggots

Length of culture significantly influenced proximate composition of housefly maggot meal (HMM). Protein content significantly reduced as the length of culture increased. Conversely, fat and fibre contents significantly increased with increased length of culture (Table 3). Protein content was highest in maggots harvested on day three and least in those harvested on day five post oviposition. However, contents of fat, fibre and ash were highest in maggots harvested on day five and least in maggots harvested on day three. Furthermore, maggots harvested on day five appeared to be creamy compared to those harvested on either day three or four.

Effect of mass of substrate on yield of maggots

Mass of substrate had an influence on maggot wet yield as shown in Table 4. Doubling of substrate mass from 12 to 24 kg led to a significant increase in maggot yield by 27%.

Discussion

The large wet yield obtained using the developed culture units in the present study could be linked to ease of harvesting by making use of photosensitivity nature of the housefly maggots. Inherently, housefly maggots react negatively to light, a condition that can be used to separate them from the substrates. Extraction of housefly larvae with the aid of light has also been demonstrated by Čičková et al (2012) who used collection trays to separate larvae from pig manure and Ezewudo et al (2015) who used mobile aluminium maggotry to culture and separate larvae from poultry manure. Wet yields obtained in this study compares favourably with those by Ezewudo et al (2015) who reached a production of 230 g/kg using mobile aluminium maggotry. Therefore, the use of developed culture units suggests that harvesting of housefly maggots was even easier than sifting through the substrates.

The significantly high wet yield of maggots using cattle offal could be attributable to nutritional quality of the substrate (Newton et al 2014), which supports the survival and growth of the larvae. Newton et al (2014) reported that culture media of animal origin possess markedly higher nutrient content in terms of protein, minerals and vitamins which can be easily assimilated by larvae and attaining biomass of 100 - 400 g/kg. Similar higher wet yields of maggot have also been observed using fish offal (Koné et al 2017) and cattle blood (Anene et al 2013). There is also possibility that the higher wet yield of maggot from cattle offal observed in this study was probably due to its long lasting odor and moisture (Nzamujo 2001; Agbeko et al 2014) which strongly attracted the flies to oviposit. Agbeko et al (2014) and Nzamujo (2001) reported that the more the quantity and long lasting moisture and odor of substrate, the more number of flies attracted to lay their eggs and the greater the number of maggots produced. Thus, where cattle offal is readily available is the most suitable culturing substrate for production of housefly maggots.

Despite good performance of cattle offal as a substrate, it was not used in the second trial as a suitable substrate for production of large volume of maggots. This is because cattle offal is limiting and costly, hence uneconomical for maggot production (Anene et al 2013). The limitation of cattle offal, viz. intestines and skins, for maggot production is explained by the fact that animal offal is used as high nutritious food in most human societies (Obeng et al 2015; Koné et al 2017). In context of this study, poultry manure was abundantly available at a minimal cost due to presence of commercial poultry farms within vicinity. Therefore, it was best selected as suitable substrate of culture for the scaling-up of maggot production in the second trial.

Increasing wet yield of maggots observed at an increasing length of culture from 3^rd day to 5^th day of maggot development may be explained by gradual accumulation of larval biomass over time (Liu et al 2017; Ukanwoko and Olalekan 2015) through the whole feeding process with larval development (Hussein et al 2017). Liu et al (2017) reported similar observations when they assessed metabolic changes in nutritional composition of black soldier fly from egg to adult. They observed an intense increase in the larval biomass from 1^st day to 4^th day of larval development. Similarly, when Hussein et al (2017) studied the effect of feeding behaviour on housefly larval development, substantial increase in larval biomass as the result of voracious feeding on decaying organic matters was observed during the three larval instars. It can therefore be suggested that harvesting of maggots should be done on day five post oviposition if maggots with highest wet weight are desired.

The significant increase in wet yield of maggots after doubling quantity of fresh poultry manure from 12 to 24 kg in the culturing chamber could be attributed to increased mass of substrate. Increasing manure mass probably improved space for maggot foraging. This led to more nutrients available for maggots growth (Pastor et al 2011), which is reflected by large quantities of maggots harvested. Similar increase in wet yield of maggot after increase in manure depth in the rearing bed has also been observed in maggots cultured under controlled condition (Hussein et al 2017). The same authors demonstrated that maggots explore deeper parts of substrate as nutrients become limiting at the surface over time. However, according to Koné et al (2017) it should be noted that accumulation of fresh manure mass higher than 10 cm deep can reduce the quantity of maggot wet yield due to unfavourable conditions due to increasingly anaerobic conditions caused by the rise of temperature in the composting process.

Crude protein contents of housefly maggot meal (HMM) produced during the current study were differently affected by length of culture. This corroborates earlier reports that crude protein contents of HMM fluctuate overtime during larval development (Ukanwoko and Olalekan 2015). The mean crude protein (46.69%) of HMM from all the three lengths of culture was higher than the reported average of 38.9% (Ogunji et al 2006) but within the reported range of 42.3% to 55.4% (Aniebo and Owen 2010). The observed reduction in crude protein content of HMM with increased length of culture could be attributed to a number of reasons. According to Hussein et al (2017) and Larraín and Salas (2007) as maggots grew from 1^st instar to late 3^rd instar stage, there is a gradual increase in the utilization of body protein for enzymatic reaction in the formation of chitin layer. This suggests that dissociation of body protein led to reduced crude protein content in maggots. Moreover, Horn (1998) found that the large proportion of the nitrogen in fresh poultry manure is lost with time through ammonia volatilization thus making it unavailable to larvae fed on that manure. The loss is attributed to low nitrogen values in the maggots and the ultimately low crude protein values.

Crude fat content of HMM in the current study (25.92%) falls within range 19.64% (Hussein et al 2017) and 25.35% (Aniebo and Owen 2010). The increase in crude fat content with increased length of culture could also be linked to accumulation of fat through the active feeding process with larval development. A similar increase in crude fat content was observed for black soldier fly during larval development where fat rose from 4.8% on 1st day to 28.4% on 14^th day of larval age (Liu et al 2017). Moreover, Arrese and Soulages (2010) found that insect larvae at second and third-instar stages accumulated adequate amount of fats, representing up to 50% of the dry weight, in the form of glycogen and triglyceride as stored energy for extended non-feeding period of pupal stage. This led to intense rise in crude fat content from 3^rd day to 6^th day of larval formation.

Higher ash content in HMM harvested on 5th day post oviposition could also be linked to higher level of minerals, accumulated for cuticle formation (Liu et al 2017). A similar higher ash content (10.1%) was observed in maggot meal with chopped mango attractant harvested after 120 hours of culture (Ukanwoko and Olalekan, 2015). In general, nutrient contents of the produced housefly maggot meal are adequate to be used as the major source of protein in tilapia diets.

Conclusions

• This study demonstrated that separation of housefly maggots from substrate using the developed culture unit is easy to perform and allows reasonable collection of maggots.
  
  
• Cattle offal is good substrate in supporting high wet yield of HMM, thus where easily available is the most suitable substrate for production of larger volumes of housefly maggots.
  
  
• Harvesting maggots on 3rd day post oviposition is desirable to produce HMM with highest crude protein level and with relatively lower wet weight, while harvesting maggots on 5th day post oviposition is desirable to produce HMM with highest crude fat level and relatively higher wet weight.
  
  
• Doubling substrate weight from 12 kg to 24 kg of wet poultry manure in 1.06 m2 culture bed increases housefly maggot yield.

Recommendation

Further studies need to be conducted to enable commercial availability of HMM and widen its use in efforts to improve nutritive value of fish diets. Acknowledgement The first author is very thankful for the financial support provided by the AquaFish Innovative Lab (AIL) through a project titled Development of a Sustainable Tilapia Culture in Tanzania.

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Received 10 March 2019; Accepted 15 March 2019; Published 1 April 2019

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