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In developing countries, effective waste management strategies are constrained by high collection costs and lack of adequate treatment and disposal options. The organic fraction in particular, which accounts for more than 50% of the waste production, constitutes a great, yet mostly neglected, reuse potential. Concomitantly, the demand for alternative protein sources by the livestock feed industry is sharply increasing. A technology that effectively transforms organic waste into valuable feed is therefore a timely option. Larvae of the non-pest black soldier fly, Hermetia illucens L. (Diptera, Stratiomyidae), may be used to reduce the mass of organic waste significantly. Concurrently, larval feeding converts organic waste into prepupae (last larval stage) which is high in protein. In combination with a viable market, this potential animal feed may cover the waste collection costs and thus promote innovative, small-scale entrepreneurs to establish a profitable business niche. Organic waste, however, often contains persistent pollutants, such as heavy metals, that may accumulate in the larvae and prepupae of black soldier flies and consequently in the food chain. In this study, we fed black soldier fly larvae chicken feed spiked with heavy metals (cadmium, lead and zinc at three concentrations each) to examine the extent of metal accumulation in the different life stages and the effect of heavy metal concentration in the feed on the life cycle determinants of the flies. The cadmium accumulation factor in prepupae (metal concentration in the body divided by metal concentration in the food) ranged between 2.32 and 2.94; however, the lead concentration remained well below its initial concentration in the feed. The bioaccumulation factor of zinc in prepupae decreased with increasing zinc concentration in the feed (from 0.97 to 0.39). None of the three heavy metal elements had significant effects on the life cycle determinants (prepupal weight, development time, sex ratio).
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Journal of Insects as Food and Feed, 2015; 1(4): 261-270 WageningenAcademic
Publishers
ISSN 2352-4588 online, DOI 10.3920/JIFF2015.0030 261
1. Introduction
Urban poverty is a fundamental challenge in low and
middle-income countries associated with rapid urban sprawl
(Moore et al., 2003). The urban poor suffer most from
inadequate sanitary services and deficient municipal solid
waste management leading to increased health risks and
impaired household resilience. While informal collection
and recycling systems of inorganic material with a market
value are currently available, the organic waste fraction
often remains uncollected and untreated. Indiscriminately
dumped organic waste accumulates along streets, clogs
stormwater drains, pollutes water bodies, rots, and attracts
disease-transmitting vectors (e.g. flies, rodents), thus posing
serious direct or indirect health risks to local residents.
Local authorities, community-based organisations, non-
governmental organisations and research institutions
have recognised this deficiency and identified the need
for simple, environmentally and economically sustainable
organic waste treatment solutions in urban areas (Fluitman,
2000; Zurbrügg et al., 2007).
In many low and middle-income countries, the mass of
organic waste may be substantially reduced using larvae of
the non-pest black soldier fly, Hermetia illucens L. (Diptera:
Stratiomyidae) (Diener et al., 2009). H. illucens larvae feed
Bioaccumulation of heavy metals in the black soldier fly, Hermetia illucens and effects
on its life cycle
S. Diener1*, C. Zurbrügg1 and K. Tockner1,2,3
1
Eawag: Swiss Federal Institute of Aquatic Science and Technology, P.O. Box 611, 8600 Dübendorf, Switzerland;
2
IGB,
Leibniz-Institute for Freshwater Ecology and Inland Fisheries, Mueggelseedamm 310, 12587 Berlin, Germany; 3Freie
Universität Berlin, Institute of Biology, Takustrasse 3, 14195 Berlin, Germany; stefan.diener@eawag.ch
Received: 25 December 2014 / Accepted: 22 May 2015
© 2015 Wageningen Academic Publishers
RESEARCH ARTICLE
Abstract
In developing countries, effective waste management strategies are constrained by high collection costs and lack
of adequate treatment and disposal options. The organic fraction in particular, which accounts for more than 50%
of the waste production, constitutes a great, yet mostly neglected, reuse potential. Concomitantly, the demand
for alternative protein sources by the livestock feed industry is sharply increasing. A technology that effectively
transforms organic waste into valuable feed is therefore a timely option. Larvae of the non-pest black soldier
fly, Hermetia illucens L. (Diptera: Stratiomyidae), may be used to reduce the mass of organic waste significantly.
Concurrently, larval feeding converts organic waste into prepupae (last larval stage) which is high in protein. In
combination with a viable market, this potential animal feed may cover the waste collection costs and thus promote
innovative, small-scale entrepreneurs to establish a profitable business niche. Organic waste, however, often contains
persistent pollutants, such as heavy metals, that may accumulate in the larvae and prepupae of black soldier flies and
consequently in the food chain. In this study, we fed black soldier fly larvae chicken feed spiked with heavy metals
(cadmium, lead and zinc at three concentrations each) to examine the extent of metal accumulation in the different
life stages and the effect of heavy metal concentration in the feed on the life cycle determinants of the flies. The
cadmium accumulation factor in prepupae (metal concentration in the body divided by metal concentration in the
food) ranged between 2.32 and 2.94; however, the lead concentration remained well below its initial concentration
in the feed. The bioaccumulation factor of zinc in prepupae decreased with increasing zinc concentration in the feed
(from 0.97 to 0.39). None of the three heavy metal elements had significant effects on the life cycle determinants
(prepupal weight, development time, sex ratio).
Keywords: bioaccumulation, developing countries, food security, organic waste management, protein
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S. Diener et al.
262 Journal of Insects as Food and Feed 1(4)
voraciously on decaying organic leftovers from markets
and restaurants, animal droppings and on human faeces.
Myers et al. (2008) and Sheppard et al. (1994) reported a
33-58% reduction in organic matter from cow manure and
50% from chicken manure respectively and Diener et al.
(2011) reached a dry matter reduction of 70% in municipal
organic waste.
The final larval instar of H. illucens is called the prepupa
and consists of 32-44% raw protein and 33-35% crude fat
(Booram et al., 1977; Diener et al., 2009; St-Hilaire et al.,
2007). Hence, larval feeding converts organic waste into
a highly valuable protein that may be used as a substitute
for fishmeal. The increase in aquaculture led to a growing
demand for feed for aquatic organisms and therefore to
increasing prices (Riddick, 2014). Fishmeal is becoming
less available and the production and the sale of insect
protein can thus contribute to cover the waste collection
costs as well as allow innovative, small-scale entrepreneurs
to establish a profitable business niche.
However, organic waste often contains persistent pollutants
such as heavy metals that may accumulate in larvae and
prepupae and therefore enter the food chain. The heavy
metals enter the waste stream in various ways, be it through
atmospheric emissions or inappropriate disposal of heavy
metal containing refuse. While terrestrial organisms
ingest contaminants orally (biomagnification), aquatic
organisms also enrich pollutants in their biomass through
diffusion (bioconcentration). Bioaccumulation refers to
both bioconcentration and biomagnification (Walker, 1990).
The bioaccumulation factor (BAF) thus is the concentration
of a pollutant in organisms divided by its concentration
in the diet.
A stable black soldier fly population generating viable
eggs and producing healthy offspring are prerequisites
for running a sustainable organic waste treatment facility
using black soldier flies. However, heavy metals in organic
waste may influence life history traits. For example copper-
and lead-contaminated host plants negatively affected
fecundity and intrinsic rate of natural increase (rm) in the
cabbage aphid, Brevicoryne brassicae L. (Görür, 2006).
Reduced bodyweight in the offspring of the carabid beetle,
Pterostichus oblongopunctatus, inhabiting a metal-polluted
environment has been observed by Lagisz and Laskowski
(2008) and Moroń et al. (2014) found a clear relation
between increasing metal concentrations in the soil layer
and the increased negative impact on life cycle determinants
(e.g. population growth rate, number of brood cells, survival
rate) for wild bees, Osmia rufa.
In this study, the larvae of the black soldier fly, H. illucens,
were fed with chicken feed contaminated by different levels
of cadmium, lead and zinc to investigate the following
research questions:
•
To what extent do cadmium, lead and zinc – fed at
different concentrations – accumulate in the prepupae
of the black soldier fly?
•
Does heavy metal in the food influence the life cycle
determinants of the flies? (i.e. development time, body
weight, sex ratio)?
2. Materials and methods
Animals
Black soldier flies, H. illucens L. (Diptera: Stratiomyidae),
were obtained from a laboratory colony grown in an indoor
cage (1.5 m × 1.5 m × 2.0 m) at constant temperature
(26.5±0.05°C, 60.8±0.8% RH). The room was fitted with
two windows as direct sunlight is crucial for successful
mating (Tomberlin and Sheppard, 2002).
The newly hatched larvae used for the experiments were
reared on chicken feed (UFA 625, digestible energy:
11.7 MJ/kg, 60% moisture). A detailed description of the
rearing and hatching facility is given in Diener et al. (2009).
The experiments conducted in Switzerland did not violate
Swiss law (e.g. Animal Protection Law, Animal Husbandry
Act) or any of the provisions or regulations stipulated in
these laws. The experiments also met the International
Guiding Principles for Biomedical Research Involving
Animals as issued by the Council for the International
Organizations of Medical Sciences (CIOMS, 1985).
Experimental setup
Larvae were fed with chicken feed pellets moistened (final
moisture level: 60%) with either pure deionised water
(control) or a solution of deionised water containing heavy
metal ions (three concentration levels for each metal).
The 2% HNO
3
solutions used for feedstock preparation
contained cadmium (1000 mg/kg), lead (1000 mg/kg) or
zinc (10,000 mg/kg). The nominal concentrations in the
food were: 0.0 μg/g (control), 2.0, 10.0, and 50.0 μg/g Cd;
0.0 μg/g (control), 5.0, 25.0, and 125.0 μg/g Pb; 0.0 μg/g
(control), 100, 500, and 2,000 μg/g Zn. Low concentrations
corresponded to the metal concentrations typical for
market vegetables in India or Bangladesh (Alam et al.,
2003; Marshall et al., 2003; Sharma et al., 2007). Middle
concentrations for cadmium and lead corresponded to
concentrations typical for organic waste in Bangladesh or
Sweden (Eklind et al., 1997; Rytz, 2001) (Table 1).
Metal concentrations in the control groups were
derived from the chicken feed itself. Unfortunately, the
experiment series with the low concentrations of zinc were
contaminated and the results had to be discarded. However,
as the chicken feed itself had similar concentrations of zinc
(145.3 mg/kg, standard error (SE) = 10.1) as what was used
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Bioaccumulation of heavy metals in black soldier fly
Journal of Insects as Food and Feed 1(4) 263
in the experiment with low concentrations (177.4 mg/kg,
SE=3.8) we were able to utilise the control series (only
chicken feed and its respective zinc concentration) as
indication of results for the low zinc concentration series.
Thus the control series could be considered as the low zinc
concentration series and was compared to the medium
and high zinc series.
Each replicate (three replicates per treatment) contained
200 7-day old larvae placed in plastic containers (14.0 × 7.5
× 7.0 cm) and covered with nylon tulle held in place by the
lid of the box. The lids with nine holes (ø 15 mm) allowed
air circulation. The food and larvae were covered with a
re-sealable polyethylene bag containing a piece of black
cardboard to shield larvae from light. The pre-prepared
meal portions were packed into separate polyethylene bags
and kept frozen until use. The quantity of the diet was
calculated based on 100 mg food (wet weight) per larva
and day. The larvae were fed three times a week. Feeding
stopped when 50% of the larvae in the box metamorphosed
into prepupae to avoid overfeeding the remaining larvae.
Sampling and analysis
The samples (larvae, larval exuviae, prepupae, pupal exuviae,
and adults) were washed with deionised water, weighed,
lyophilised to measure dry weight, and ground in an agate
mortar for heavy metal analysis. The food samples and the
remains at the end of the experiments, the so-called residue,
were treated the same way except for the washing. Larvae
and prepupae were killed by freezing (-10°C), while adults
were killed with ethyl acetate. To prepare the samples for
the analyses, ~50 mg of the ground material was digested
in polytetrafluoroethylene beakers (HPR-300/10; MLS
GmbH, Leutkirch im Allgäu, Germany). The material was
moistened with deionised water. Approximately 4 ml HNO
3
and 1 ml H
2
O
2
were added before the sample was heated in
a laboratory microwave digester (MLS 1200 MEGA; MLS
GmbH). The clear solution was diluted with deionised
water (10× for Cd and 100× for Pb and Zn) and analysed
with the high resolution inductively coupled plasma-mass
spectrometer (HR-ICP-MS, Element II; Thermo Fisher
Scientific, Waltham, MA, USA). The standard solutions
were made using Merck ICP multi-element standard
solution IV (Merck Millipore, Darmstadt, Germany): 10,
100, 1000, 5,000 and 10,000 ng/l. The natural river water
standard SLRS-4 and the TM-28.3 trace elements fortified
calibration standard (National Research Council Canada,
Ottawa, Canada) were used as a control. The detection
limit for these elements was 10 ng/l.
BAF was calculated according to Walker (1990) as:
concentration in organism (Ci)
BAF = (1)
concentration in food and/or water ingested (Co)
In the present case, Co consisted solely of the heavy metal
concentration in the food.
Table 1. Heavy metal concentration in municipal solid waste and vegetables (based on dry weight) compared to the legal maximum
threshold level allowed in animal feed, human food and compost.1
Cadmium (mg/kg) Lead (mg/kg) Zinc (mg/kg) Reference
Heavy metal concentration in municipal solid waste
Sweden 0.16-0.6 2.4-26 49-165 Eklind et al., 1997
Dhaka, Bangladesh 5.0 n/a 226 Rytz, 2001
Heavy metal concentration in vegetables
Garden vegetables, rural village, Bangladesh 0.05-0.4 0.2-1.7 11-54 Alam et al., 2003
Market vegetables, Delhi, India 1.0-5.5 0.3-2.2 41-150 Marshall, 2003
Field vegetables, Varanasi, India 0.5-4.3 3-16 3-41 Sharma et al., 2007
Heavy metal limits in animal feed
European Union 2 10 n/a EC, 2002
Heavy metal limits in human food
European Union 0.05-1.0 0.02-1.0 n/a EC, 2001
India 0.1-1.5 0.2-10 5-100 Government of India, 1954
Heavy metal limits in compost from household waste
European Union 0.7 45 200 EC, 1991
Proposed standard in LMIC 3 150 300 Hoornweg et al., 1999
1 LMIC = low and middle-income countries; n/a = not applicable.
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S. Diener et al.
264 Journal of Insects as Food and Feed 1(4)
Statistical analyses
Statistical analyses were performed using SPSS Statistics
17.0 software (SPSS Inc., Chicago, IL, USA). For some
data, a violation of the Levene homogeneity of variances
was calculated. However, as the groups are equal in size,
ANOVA is very robust to this violation.
3. Results
Heavy metal accumulation
In all development stages (larvae, prepupae, and adults),
the metal concentration generally increased significantly
with increasing metal concentration in the food (Table 2-5).
However, BAF, i.e. the ratio of the amount of metal in
the body compared to that in the food varied among the
different metal elements and development stages (Table 6).
In prepupae, the BAF ranged from 2.32 to 2.94 for cadmium,
independent of the concentration in the food, while the
BAF remained <1 (0.25-0.74) for lead. In adults, the BAF
was very low for both cadmium and lead concentrations
(BAF=0.12-0.21). For zinc, the BAF decreased with
increasing concentration in the food (prepupae: from 0.97
to 0.39; adults: from 0.98 to 0.19). The EU threshold value
for cadmium (2 mg/kg) in animal feed was exceeded in
prepupae even at low cadmium concentration (7.9 mg/kg,
SE=0.6). Only prepupae from the low lead concentration
group (1.5 mg/kg, SE=0.7) met the EU concentration limit
for lead (10 mg/kg) in animal feed (EC, 2002).
Table 2. Cadmium concentration in soldier flies, Hermetia illucens, at different life stages based on dry weight, in digested material
(residue) and in food source. Larvae fed with chicken feed (100 mg/larva/day, 60% moisture) spiked with cadmium (three different
concentrations).1,2
Control Low cadmium Medium cadmium High cadmium
Mean (mg/kg) SE Mean (mg/kg) SE Mean (mg/kg) SE Mean (mg/kg) SE
Food 0.2 a 0.02 2.7 b 0.2 13.3 b 0.7 61.5 b 2.3
Residue 0.2 a 0.01 2.9 b 0.1 16.0 bc 0.4 89.8 c 2.1
Larvae 0.2 a 0.02 7.0 d 0.3 32.5 d 0.6 170.5 d 8.5
Prepupae n.d. 7.9 d 0.6 36.2 d 1.9 142.9 e 8.3
Adults n.d. 0.6 a 0.04 1.9 a 0.2 7.8 a 0.4
Larval exuviae 0.1 a 0.03 2.2 ab 0.3 18.8 bc 4.1 54.2 b 3.7
Pupal exuviae 0.5 b 0.1 5.2 c 0.7 22.9 c 2.6 94.1 c 12.1
1 Mean values followed by the same small letter in the same column do not vary significantly (P>0.05).
2 SE = standard error; n.d. = not detected.
Table 3. Lead concentration in soldier flies, Hermetia illucens, at different life stages based on dry weight, in the digested material
(residue) and in food source. Larvae fed with chicken feed (100 mg/larva/day, 60% moisture) spiked with lead at three different
concentrations.1,2
Control Low lead Medium lead High lead
Mean (mg/kg) SE Mean (mg/kg) SE Mean (mg/kg) SE Mean (mg/kg) SE
Food 1.1 ab 0.4 5.9 bc 0.3 34.3 c 1.8 142.9 b 2.9
Residue 0.1 a 0.01 7.8 cd 0.6 53.2 d 3.3 267.9 c 12.8
Larvae n.d. 3.8 ab 0.4 22.8 b 1.6 141.7 b 17.2
Prepupae n.d. 1.5 a 0.7 25.3 bc 1.9 40.1 ab 3.7
Adults n.d. n.d. 5.9 a 0.57 17.3 a 1.36
Larval exuviae 5.9 c 1.3 11.3 e 0.01 87.7 e 4.8 312.9 c 74.1
Pupal exuviae 3.7 bc 0.1 9.3 de 1.0 24.2 bc 2.1 66.7 ab 3.6
1 Mean values followed by the same small letter in the same column do not vary significantly (P>0.05).
2 SE = standard error; n.d. = not detected.
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Bioaccumulation of heavy metals in black soldier fly
Journal of Insects as Food and Feed 1(4) 265
Effects of heavy metals on life cycle determinants
Prepupae treated with cadmium were significantly heavier
than the control group. No significant effects were found in
prepupae treated with lead and zinc (Table 7). Development
time from hatching of the larva to the prepupal stage
generally increased with heavy metal concentration
although the increase was statistically insignificant (Table 8).
Average development time until pupation amounted to
15.2 days (SE=0.1) and did not differ significantly between
treatments or sexes. Heavy metals had no influence on
the sex ratio of adults (average males/females ratio: 0.98,
SE=0.02).
4. Discussion
The black soldier fly, H. illucens, fed with cadmium, lead
and zinc, exhibits different accumulation patterns. Larvae
and prepupae accumulated cadmium, yet the incorporation
of lead and zinc was suppressed as concentrations found in
the body were lower than in the food. These findings are
consistent with literature data (Figure 1). In the literature
reports, the BAF of cadmium uptake by detritivorous insects
averages 2.86 (SE=0.30, range 0.46-6.09) (Gintenreiter et
al., 1993; Kazimirova and Ortel, 2000; Kramarz, 1999;
Lindqvist, 1992; Maryanski et al., 2002; Ortel, 1995).
Cellular cadmium uptake probably occurs through Ca2+
channels. Due to their very similar ionic radii, Cd
2+
ions
can easily enter the cell via Ca
2+
channels, independent of
endocytosis or an ATP requiring ion pump (Braeckman
et al., 1999). Moreover, Braeckman et al. (1999) found a
protein of the HSP70-family induced by elevated cadmium
concentrations in the environment of Aedes albopictus
(Diptera: Culicidae) cells. Production of this protein, which
protects other proteins from denaturation, may also explain
the low effect of contaminated food on life-cycle parameters
such as development time or fluctuating asymmetry despite
the observed bioaccumulation of cadmium (cf. present
study).
Table 4. Zinc concentration in soldier flies, Hermetia illucens, at different life stages based on dry weight, in the digested
material (residue) and in food source. Larvae fed with chicken feed (100 mg/larva/day, 60% moisture) spiked with zinc at three
different concentrations. Samples from the series ‘Low zinc’ were contaminated during the experiment and could not be used
for interpretation.1,2
Control Low zinc Medium zinc High zinc
Mean (mg/kg) SE Mean (mg/kg) SE Mean (mg/kg) SE Mean (mg/kg) SE
Food 145.3 b 10.1 177.4 3.8 616 b 37.8 2,044 c 16.2
Residue 192.3 b 13.1 n/a 1,196 c 66.7 3,313 d 240.9
Larvae 165.8 b 19.9 n/a 596 b 88.0 866 b 141.9
Prepupae 138.9 b 24.3 n/a 513 ab 44.5 801 ab 32.1
Adults 141.4 b 9.2 n/a 272 ab 22.8 389 ab 37.6
Larval exuviae 275.5 c 13.5 n/a 1,514 c 240.2 1,883 c 104.8
Pupal exuviae 35.1 a 4.1 n/a 145 a 39.2 334 a 56.5
1 Mean values followed by the same small letter in the same column do not vary significantly (P>0.05).
2 SE = standard error; n/a = not applicable.
Table 5. Kendall’s tau rank correlation (r) between the heavy metal concentration in food and the concentration values in larvae,
prepupae, larval exuviae, and adults of the black soldier fly, Hermetia illucens.
Larvae Prepupae Larval exuviae Adults
r P N r P N r P N r P N
Cadmium 0.778* 0.004 12 0.833* 0.002 9 0.722* 0.007 9 0.741* 0.000 18
Lead 0.778* 0.004 9 0.833* 0.002 9 0.778* 0.004 9 0.671* 0.001 17
Zinc 0.667* 0.012 9 0.611* 0.022 9 0.833* 0.002 9 0.647* 0.000 18
* P<0.05
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S. Diener et al.
266 Journal of Insects as Food and Feed 1(4)
Table 6. Bioaccumulation factor (BAF) for larvae, prepupae and adults of the black soldier fly, Hermetia illucens, fed heavy
metal contaminated food at three different concentrations (low, medium and high; Table 2, Table 3 and Table 4). BAF for ‘low
concentration, zinc’ was calculated using data from the control group (see explanation in text). Because the concentrations of
cadmium and lead in the control group were so low, the analytical error had the effect of providing inaccurate BAFs, and are
therefore not shown here.1
Low Medium High
BAF SE BAF SE BAF SE
Cadmium
Larvae 2.65 0.10 2.46 0.11 2.79 0.24
Larval exuviae 0.86 0.19 1.41 0.31 0.88 0.06
Prepupae 2.94 0.09 2.75 0.25 2.32 0.09
Adults 0.21 0.01 0.15 0.01 0.13 0.01
Lead
Larvae 0.66 0.09 0.67 0.07 0.99 0.10
Larval exuviae 1.9 0.11 2.56 0.01 2.21 0.56
Prepupae 0.25 0.12 0.74 0.03 0.28 0.03
Adults n/a 0.17 0.01 0.12 0.01
Zinc
Larvae 1.14 0.09 0.97 0.14 0.42 0.07
Larval exuviae 1.92 0.19 2.45 0.32 0.92 0.04
Prepupae 0.97 0.20 0.84 0.09 0.39 0.01
Adults 0.98 0.08 0.45 0.04 0.19 0.02
1 SE = standard error; n/a = not applicable.
Table 7. Prepupal dry weight of Hermetia illucens fed with chicken feed (100 mg/larva/day, 60% moisture) spiked with three different
heavy metals at different concentrations (low, medium and high).1,2
Control Low Medium High
Mean (mg) SE Mean (mg) SE Mean (mg) SE Mean (mg) SE
Cadmium 55.9a 2.3 96.2c 10.0 75.3b 2.0 83.6bc 3.3
Lead 55.9ab 2.3 61.5b 6.8 51.3a 2.1 59.1ab 0.6
Zinc 55.9a 2.3 n/a 64.8a 5.7 59.2a 4.8
1 Mean values followed by the same small letter in the same row do not vary significantly (P>0.05).
2 SE = standard error; n/a = not applicable.
Table 8. Effects of heavy metal concentration (low, medium and high) in food on development time (eclosion from egg to prepupa)
of Hermetia illucens larvae.1,2
Control Low Medium High
Mean (days) SE Mean (days) SE Mean (days) SE Mean (days) SE
Cadmium 18.4ab 0.5 18.0a 0.5 18.8ab 0.4 19.3b 0.6
Lead 18.4a 0.5 18.8ab 0.3 19.4b 0.4 20.7c 0.2
Zinc 18.4a 0.5 n/a 18.9a 0.5 20.1b 0.6
1 Mean values followed by the same small letter in the same row do not vary significantly (P>0.05).
2 SE = standard error; n/a = not applicable.
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Bioaccumulation of heavy metals in black soldier fly
Journal of Insects as Food and Feed 1(4) 267
In contrast to cadmium, the BAF for zinc decreased with
increasing zinc concentration in the food, which suggests
active regulation of zinc within the body (Table 6). Similarly,
larvae of the house fly, fed with zinc-contaminated food
(from 61 to >7,000 mg/kg) accumulated zinc only up to a
maximum level of 216 mg/kg (Kramarz, 1999; Maryanski
et al., 2002). Even though the mean zinc concentration
in the literature data for Musca domestica is lower than
that found in prepupae of H. illucens of the present study
(484 mg/kg, SE=97.5), it is possible that the two organisms
possess a similar regulation mechanism.
Active regulation of zinc in insects has been described
previously (Lindqvist, 1995; Mason et al., 1983). Zinc is
an essential, yet potentially toxic element. Therefore, it
is not surprising that its intracellular uptake is actively
regulated. Especially the metal-responsive-element-binding
transcription factor-1 (MTF-1) is a key regulator in higher
4
3
2
1
00.1 1 10 100 1000
Bioaccumulation factor (BAF)
Cadmium
0 100 200 300 400 500
200
150
100
50
0
500
400
300
200
100
0
0 50 100 150 200
Cadmium
Concentration sample (mg/kg)
Concentration sample (mg/kg)
4
3
2
1
0
110 100 1000
Bioaccumulation factor (BAF)
LeadLead
0 500 1000 1,500 2,000
2,000
1,500
1000
500
0
Concentration food (mg/kg)
Zinc
Concentration sample (mg/kg)
4
3
2
1
0
10 100 1000
Concentration food (mg/kg)
Bioaccumulation factor (BAF)
Zinc
Figure 1. Concentration and bioaccumulation factor (BAF) of heavy metals in black soldier fly larvae (○) and prepupae (●), which
were fed with heavy metal spiked food (current study). Crosses show data from literature which originates from similar studies about
heavy metal concentrations in various insect larvae (Cd: Kazimirova and Ortel, 2000; Kramarz, 1999; Lindqvist, 1992; Maryanski
et al., 2002; Ortel, 1995; Pb: Gintenreiter et al., 1993; Kazimirova and Ortel, 2000; Ortel, 1995; Zn: Kramarz, 1999; Maryanski et al.,
2002). 1:1 line shown for reference. Missing BAF values are attributed to undetectable concentrations in control groups.
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S. Diener et al.
268 Journal of Insects as Food and Feed 1(4)
eukaryotic cells. It is responsible for the activation of several
genes involved in intracellular zinc sequestration and
transport (Laity and Andrews, 2007).
Though larvae and prepupae contained low lead
concentrations in the present study, the larval exuviae
accumulated lead. Lead tends to be stored in granular,
metal-containing structures of the cells before it is
transported to and immobilised in the exoskeleton (Hare,
1992). Similar to terrestrial insects, lead is most likely
disposed of during moulting (Roberts and Johnson, 1978).
Heavy metal concentration in adults was significantly lower
than in prepupae. We assume that this phenomenon occurs
mainly because animals defecate before pupation or shortly
after adult emergence. Yet Sheppard et al. (1994) reported
without supporting data that prepupae had an empty gut
when migrating. Conversely, Aoki and Suzuki (1984)
describe an over 50% loss of the larva’s cadmium content
due to defecation in newly emerged flesh flies within the
first two days following emergence. In the present study,
prepupae were collected 1-3 days after transformation. We
assume that defecation had not occurred during this period,
and cadmium was removed during the later prepupal phase,
i.e. during pupation, or after emergence. Therefore, toxic
substances and pathogens present in the waste may remain
in the gut of the harvested prepupae and in this way may be
taken up by fishes or poultry fed with the prepupae. Future
studies have to determine the period between initiation of
the last larval instar (prepupa) and defecation, including the
potential loss of feedstuff energy due to such a protraction.
The effective elimination of heavy metals by defecation
has been described for larvae of the social paper wasp
Polistes dominulus (Hymenoptera: Vespidae) (Urbini et
al., 2006). However, even if heavy metals accumulate in the
cells lining the alimentary canal, they may be rejected after
a short time. For example, Tenebrio molitor (Coleoptera:
Tenebrionidae) discards cells of the midgut epithelium
after four days (Lindqvist and Block, 1995; Thomas and
Gouranto, 1973). Heavy metal accumulated in these cells
will therefore be rejected with defecation.
5. Conclusions
Our studies reveal that the concentrations of lead and zinc
in larvae or prepupae remain below the initial amounts in
the food. Furthermore, the three heavy metal elements
examined had only minor effects on the development of
the black soldier fly even at very high concentrations. Yet,
since cadmium accumulated in the prepupae, it could
potentially limit the use of prepupae in the production of
animal feed. In the case of lead and zinc, concerns about
the use of prepupae in animal feed are less critical. The
waste treatment technology using black soldier flies may
contribute to reducing the burden of an animal protein
shortage in the animal feed market and provide new income
opportunities for small entrepreneurs in low and middle-
income countries.
Acknowledgements
We wish to express our thanks to Simone Blaser and
Mauro Esposito for assisting during the experiments,
David Kistler for supporting us in lab analysis and Alejandra
Teresita Arroyo for her statistical advice. We appreciate
the comments by Janet Hering on an early version of the
manuscript, and are grateful to Sylvie Peter for linguistic
editing support. The authors would like to acknowledge the
financial support by the Velux Foundation, Eawag: the Swiss
Federal Institute of Aquatic Science and Technology, the
Swiss National Centre of Competence in Research (NCCR
North South) and the Swiss Agency for Development and
Cooperation (SDC).
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... Tschirner y Simon (2015), señalan que existe relación entre el sustrato y contenido en minerales, en cambio, Spranghers y colaboradores (2017), no señalan esta relación. En cuanto a los patrones de acumulación a lo largo de las etapas de desarrollo, solo han sido estudiados en profundidad para metales pesados potencialmente peligrosos, como el Cd y el Pb Maryansky, et al., 2002;Diener 2011;Diener 2015;Wang, et al., 2018). Sin embargo, es conocido que el contenido nutricional de los insectos es altamente variable (Rumpold y Schluter, 2013;Finke, 2015), incluso dentro de la misma especie en función del tipo de sustrato de cría. ...
... El comportamiento y los patrones de acumulación de minerales y metales pesados, varían según el elemento químico, la concentración inicial en el alimento, y el estado de desarrollo del insecto (Devkota, et al., 2000;Gyliene yy Salkauskas, 2002;Zhuang, 2008;Zhang, et al, 2009;Diener, 2011Diener, , 2015EFSA, 2015;Bulak, et al., 2018;Schorogel y Watjen, 2019;Smonroo, et al., 2019;Imathiu, 2020;Wu, et al., 2020). Desde el punto de vista de la toxicidad, el metal que presenta un mayor riesgo por su acumulación en productos alimenticios, es el Cd Maryansky, et al., 2002;Wang, et al., 2018;Sarpong, et al., 2019;Imathiu, 2020). ...
...  No parecen presentar ningún mecanismo de regulación de elementos no esenciales como Cd, Pb, Hg y As, y, por tanto, existe una correlación positiva entre la concentración del metal en el sustrato y la concentración en la biomasa del insecto (Maryanski, et al., 2002;Biancarosa, et al., 2018;Diener, et al., 2015). ...
Thesis
Full-text available
The foreseeable increase in the world population, estimated for the year 2050 in 9,500-10,000 million people, will be one of the main challenges facing the 21st century. In addition to the necessary resources and inputs (space, water, waste, etc.), the food safety of the planet will lead to a high demand for protein, both for animal feed and for human nutrition. Our main sources of protein come from agriculture, livestock (including aquaculture) and fishing. It is for this reason that the production and performance of domesticated plants and animals has increased exponentially over the last decades, currently being very close to their biological limits. However, this high efficiency is inversely related to the environmental sustainability of these production systems. Among the consequences, the production of highly nutritious compound feed has also increased. For its elaboration, large amounts of fish flour and oil, as well as soy, among other components, are necessary. The intensive cultivation of soybeans has serious environmental problems. On the other hand, the marine environment is increasingly deteriorated as a result of pollution derived from human activity and overexploitation of fishing. All of this has led to long-term economic instability and a continued rise in the prices of these raw materials. But, is it technically possible to maximize the sustainability of these production systems, simultaneously optimizing the essential economic efficiency? With this objective, it is necessary to search for new sources of proteins that can be used as ingredients in the elaboration of compound feeds intended for animal feed and indirectly for human nutrition. One of the most promising, is the obtaining of animal protein from the biomass of certain species of domesticated insects. In particular, the use of insect proteins and fats on an industrial scale will significantly improve the sustainability and efficiency of terrestrial livestock and aquaculture. Indirectly, it will allow fishing levels to be kept at rational levels and the derived by-products have great agronomic value as natural origin fertilizers. Among the most plausible candidates, diptera (Insecta: Diptera) present biological and nutritional characteristics that make them good candidates for production on an industrial scale. One of the most promising species is the black soldier fly Hermetia illucens (Linnaeus, 1758) which, together with the coleopteran Tenebrio molitor Linnaeus, 1758, currently constitute the main members of this new production sector. The European Union has also approved the use of other five species of insects as ingredients in animal feed, standing out among these the common fly Musca domestica Linnaeus, 1758. Other species of Diptera are not yet approved for this purpose, but they are also very interesting because of their great potential for artificial breeding, such as the Calliphoridae species Lucilia sericata (Meigen, 1826) or Chrysomya megacephala (Fabricius, 1794). Among the components that are part of compound feed, minerals represent an important limiting group from a nutritional point of view. Through an optimal supply of minerals, the performance of livestock production can be considerably increased at low cost. However, the levels of these compounds must be kept within certain levels determined by the legislation, to avoid nutritional problems or cause harmful effects on animal and human health. In this sense, there are very few studies about the mineral profiles of the insect biomass in general, and in particular of the black soldier fly and other species of diptera. Data about the influence that the composition of the larvae development substrate can exert, as well as its importance in the different stages of development of the life cycle. On the other hand, there is the possibility of bioaccumulation of heavy metals in the insect biomass through ingestion. Thus, due to its high toxicity, there are various studies about the concentrations of Cd and Pb in mature larvae of the black soldier fly, but there is very little information on bioaccumulation in the rest of the stages of development, as well as the possible influence of the larval rearing medium. This thesis project analyzes the possible influence of the breeding substrate on the concentrations of different minerals and heavy metals throughout the stages of the life cycle of Hermetia illucens and other species of Diptera. For this, three larval substrates with different origins were used: a) commercial laying hen feed, b) bagasse derived from beer production and c) a mixture of meat of pig origin. In the case of H. illucens, samples of prepupal larvae, pupae, puparia, prepupal exuviae and adults developed in the three development media were taken. In all cases, after drying and digestion in microwave oven, they were analyzed by induction-coupled plasma optical emission spectrometry (ICP-OES) to obtain the concentrations of Ca, Cr, Cu, Fe, K, Mg, Mn, Na, Ni and Zn, and in mass spectrometry with plasma ionization source (ICP-MS) to obtain the concentrations of Ti, Co, Sr, Mo, Cd, Sn and Pb. Few insects have the ability to develop in media of such different organic composition, therefore, as a comparative, M. domestica was bred with commercial chicken feed and beer bagasse, while Lucilia sericata and Chrysomya megacephala were developed exclusively in the meat source substrate. In this way, different types of medium processed by different types of insects and the results obtained by different species of flies with the same type of medium, could be compared. Regarding the relationships between accumulation patterns (Bioaccumulation Factor) and mineral concentrations, with the dipteran species and the substrate used, in prepupal larvae and adults no relationship is observed between results and the species or substrate, instead , the results in pupae and puparia are influenced by the study species and the feeding substrate used. On the other hand, Ca and Na behave differently in the species studied in this research. The black soldier fly has a good mineral profile for use in animal feed, comparable to fish and soybean meal. The results with house flies are also comparable to fish and soy meals, in the two media studied. The two blowflies have a lower quality mineral profile, but comparable to soybean meal and also suitable for use in the production of feed.
... (Martínez-Sánchez et al., 2011;Sheppard et al., 2002;Tomberlin et al., 2002), H. illucens can be currently found worldwide (Brammer and von Dohlen, 2007). The BSFL are voracious eaters of decayed fruits and vegetables, animal manure and municipal organic waste (MOW) (Diener et al., 2015;Paz et al., 2015;Salomone et al., 2017). Its larvae are saprophagous, have complex feeding habits, large appetite and strong resistance to the harsh environment. ...
... As a consequence, this new industry is concerned about the transfer and accumulation of these contaminants to BSFL in the feed and food chain (Lievens et al., 2021;Wang et al., 2021). More research has been carried out to establish the safety of BSFL when it is used as food and feed (Bessa et al., 2021;Diener et al., 2015;Gao et al., 2017;Makkar et al., 2014). BSFL treatment has been shown to lower the number of microorganisms in the substrate, according to prior investigations (Erickson et al., 2004;Lalander et al., 2013;Liu et al., 2008). ...
... More importantly, according to the findings of the recent research that have been completed so far, dioxins, PCBs and PAHs, as well as certain pesticides, antibiotics and mycotoxins, did not accumulate in the BSFL (Bessa et al., 2021;Bosch et al., 2017;Lalander et al., 2016;Lievens et al., 2021;Peguero et al., 2021;Purschke et al., 2017;van der Fels-Klerx et al., 2020). Cadmium, lead and zinc had no influence on the physiology of BSFL, although cadmium was shown to accumulate in the body (Diener et al., 2015). Further research found that heavy metals, particularly cadmium and lead, had a negative impact on the development, and these metals accumulated in high concentrations in the BSFL that exceed maximum permissible limits of animal feed regulations (Lievens et al., 2021;Purschke et al., 2017;Wu et al., 2020). ...
Article
Full-text available
The application of black soldier fly (BSF), Hermetia illucens based technology to process organic wastes presents a practical option for organic waste management by producing feed materials (protein, fat), biodiesel, chitin and biofertilizer. Therefore, BSF organic wastes recycling is a sustainable and cost-effective process that promotes resource recovery, and generates valuable products, thereby creating new economic opportunities for the industrial sector and entrepreneurs. Specifically, we discussed the significance of BSF larvae (BSFL) in the recycling of biowaste. Despite the fact that BSFL may consume a variety of wastes materials, whereas, certain lignocellulosic wastes, such as dairy manure, are deficient in nutrients, which might slow BSFL development. The nutritional value of larval feeding substrates may be improved by mixing in nutrient-rich substrates like chicken manure or soybean curd residue, for instance. Similarly, microbial fermentation may be used to digest lignocellulosic waste, releasing nutrients that are needed for the BSFL. In this mini-review, a thorough discussion has been conducted on the various waste biodegraded by the BSFL, their co-digestion and microbial fermentation of BSFL substrate, as well as the prospective applications and safety of the possible by-products that may be generated at the completion of the treatment process. Furthermore, this study examines the present gaps and challenges on the direction to the efficient application of BSF for waste management and the commercialization of its by-products.
... The bioconversion properties of BSFL have been studied in different agricultural wastes (Gao et al. 2019;Hasnol et al. 2020;El-Dakar et al. 2021). Diener et al. (2015) studied the bioaccumulation of Zn, Cd and Pb in the larvae, prepupae and adults of black soldier fly under the pressure of different concentrations, and the results showed that Cd would accumulate in larvae, while Zn and Pb would be excreted. Moreover, the growth environment containing high concentration of these three heavy metals minimally affected the development of black soldier fly (Diener et al. 2015). ...
... Diener et al. (2015) studied the bioaccumulation of Zn, Cd and Pb in the larvae, prepupae and adults of black soldier fly under the pressure of different concentrations, and the results showed that Cd would accumulate in larvae, while Zn and Pb would be excreted. Moreover, the growth environment containing high concentration of these three heavy metals minimally affected the development of black soldier fly (Diener et al. 2015). During the growth of black soldier fly from V instar larvae to prepupae, the contents of minerals and taurine in the body increased, whereas the contents of toxic heavy metals decreased (Giannetto et al. 2020). ...
... During the growth of black soldier fly from V instar larvae to prepupae, the contents of minerals and taurine in the body increased, whereas the contents of toxic heavy metals decreased (Giannetto et al. 2020). The European Commission (2002/32/EC) has established maximum concentrations of several heavy metals in animal feed, in which Cd, As and Pb are 2, 2 and 10 mg/kg, respectively (Diener et al. 2015;Giannetto et al. 2020). If the concentration of Cd in the feed for black soldier fly exceeds the EC maximum limit, it is necessary to evaluate whether the black soldier fly protein material used as part of complete feed surpasses the limit, and appropriately reduce the addition of larval protein material (Van der Fels-Klerx et al. 2016). ...
Article
Full-text available
The disposal of organic waste by the biocomposting of black soldier fly larvae (BSFL) has drawn broad attention. However, the discrepancies in heavy metal immobilization between BSFL biocomposting with different inoculation densities and aerobic composting need to be further researched. In this study, BSFL with inoculation densities of 0.08%, 0.24% and 0.40% was added to swine manure to investigate its influence on heavy metal bioaccumulation and bioavailability. The physicochemical properties, BSFL growth performance and amino acid contents were measured. The results showed that the germination index, total prepupal yield and bioavailable fraction removal rate (%) of Cr and Pb at an inoculation density of 0.40% of BSFL were the highest among all of the BSFL biocomposting groups. Although the bioaccumulation factor and heavy metal (Cd, Cr, Cu and Zn) concentrations of the BSFL body from swine manure with inoculation densities of 0.24% and 0.40% of BSFL were similar, the BSFL inoculation density of 0.40% had the best absorption effect on these heavy metals in terms of total prepupal yield. Therefore, this study provides a basis for exploring the optimal inoculation density of BSFL biocomposting to reduce the harmful effects of heavy metals in swine manure.
... Our obtained results of bioaccumulation factor of Cd (1.6 and 0.9) of Pupae-H and Pupae-W, respectively are coincident with Proc et al. [64] who presented a value 1.74 in BSF pupae, while higher bioaccumulation factors of 2.32 and 2.94 and of 5.60-5.90 have been reported by Diener et al. [65] and Bulak [8], respectively. ...
Article
Full-text available
Purpose Objective of this study is the valorisation of mass rearing waste of fruit flies from sterile insect technique facilities by black soldier flies into high quality and quantity products as a sustainable utilisation concept. Methods Different ratios of medfly rearing waste in hen feed were used for rearing black solder fly (BSF) larvae. The growth rate and insect survival were determined. Moreover, the mass gains were determined and bioconversion rates were assessed. Furthermore, the nutritional compositions of BSF pupae were analysed to evaluate the product quality. Results The omnivorous BSF larvae were highly efficient at converting digested waste into body mass as compared to the control treatment (hen feed). High weight of pre-pupae was recorded for all experimental diets. The efficacy of larvae to reach pupae ranged from 92.5 to 98.5%, while the efficacy of pupae to reach adults ranged from 81.7 to 89.0%. All experimental diets exhibited high rates of prepupal weight, metabolism and efficiency of conversion of digested food. A nutritional analysis revealed that the protein and fat contents were high, while the bioaccumulation of heavy metals was low, Conclusion Medfly rearing waste is a potential feed ingredient for the production of BSF pre-pupae and could be applied to valorise this rearing waste into high-value feed. Graphical Abstract
... According to U.S. National Library of Medicine (2022), Zn is found in cells along the body of animals, and it is necessary for proper functioning of the immune system, playing an important role in cell division and growth, wound healing, and carbohydrate breakdown. This corroborates Diener et al. (2015), whom speculated that zinc is an essential element for insect development. Furthermore, similarly to Mn, Zn is associated to chitin in the mandibles and maxillae of insects, contributing for their hardness (Schofield et al., 2002;Cribb et al., 2008). ...
Article
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Most information on the black soldier fly, Hermetia illucens (L.), is limited to its use as a biological control and waste management agent. Little is known about its mating and oviposition activities. Latency from emergence to mating and oviposition for colony-reared black soldier flies placed in a 1.5 × 1.5 × 3 m nylon cage located in a greenhouse was determined. Sixty-nine percent of mating occurred 2 d after eclosion and 70% of oviposition 4 d after eclosion. Time of day and light intensity significantly correlated with mating (r2 = 0.49; P < 0.0001), while time of day, temperature, and humidity significantly correlated with oviposition (r2 = 0.58; P < 0.0001). Latency after emergence significantly correlated with mating (r2 = 0.99; P < 0.0001) and oviposition (r2 = 0.99; P < 0.0001). A second experiment was conducted to examine oviposition preference of the black soldier fly. Adults were allowed to oviposit in Gainesville house fly, Musca domestica L., larval media with and without 5-d-old black soldier fly larvae. Based on sign non-parametric t-tests, numbers of egg clutches deposited in each treatment were not significantly different.
Chapter
This chapter reviews the published literature that addresses the potential for insect protein to be an important supplement to—or even a replacement for—fishmeal in diets for juvenile fish and crustaceans. Fishmeal is becoming a finite resource. This chapter highlights areas of opportunity for producing insects to help meet the future demand for high-quality animal protein in feed for cultured fish. The research on four key species—the black soldier fly, common house fly, silkworm moth, and yellow mealworm—serve as model insects to highlight advances. This research reveals that insects in the form of meal or pellets can provide adequate protein to replace, in part, standard fishmeal in feed for fish that are omnivorous (catfish, carp) rather than carnivorous (trout, salmon). Supplementing traditional feeds with insect meal could enhance the overall nutrition of omnivorous fish for commercial use. Cost-effective, large-scale rearing will require using artificial diets for insects. Manipulating the rearing environment and automation to reduce human labor could maximize production. The establishment of factories that are carefully designed and equipped to generate large quantities of insects to support the increasing demands for farm-reared fish is necessary.
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The organic household waste fraction originating from the Swedish municipality of Uppsala was analysed with respect to visible contaminations and chemical composition including heavy metals, using samples from 12 tonnes of material. Near infrared reflectance spectroscopy was used for selection of samples. After rotary sieving and automatic magnetic separation of the waste, another 0.8% of wet weight was sorted out manually as impurities. Of these, plastics constituted 78% and metals 12% of wet weight. The nitrogen, phosphorus and potassium concentrations of the waste were similar to other Swedish data. Cellulose constituted 15.6% of the organic matter, crude fat 15.0%, starch 13.2%, lignin 9.9%, hemicellulose 3.2% and sugar 1.6%. The concentrations of cadmium and mercury found in the sorted waste were low compared with other Swedish data, whereas the molybdenum concentration was relatively high. There were no significant trends in the material over the sampling period in the chemical characteristics analysed, despite variation between individual samples.
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Bioaccumulation is considered in aquatic systems and terrestrial organisms. In each case model systems are discussed which may be useful for the prediction of risks of bioaccumulation of lipophilic pollutants. -from Author
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Abstract Fly larvae may provide an effective method to mitigate two large and growing global concerns: the use of fish meal derived from capture fisheries in aquaculture diets and manure management in livestock and poultry facilities. A 9-wk feed trial was conducted to determine whether fly larvae could be used as a partial fish meal and fish oil replacement in rainbow trout, Oncorhynchus mykiss, diets. A trout diet was formulated to contain 40% crude protein and 15% fat. Sixty-seven percent of the protein in the control diet was derived from fish meal, and all the fat was derived from fish oil. Two of the test diets included using the black soldier fly, Hermetia illucens, prepupae, which are 40% protein and 30% fat, as 25 and 50% replacement for the fish meal component of the control diet. The total protein derived from black soldier fly prepupae in these two test diets was 15 and 34%, respectively. A third test diet included using housefly, Musca domestica, pupae, which is 70% protein and 16% fat, as 25% replacement for the fish meal component of the control diet. Data suggest that a rainbow trout diet where black soldier fly prepupae or housefly pupae constitute 15% of the total protein has no adverse effect on the feed conversion ratio of fish over a 9-wk feeding period. In addition, the diet with black soldier fly prepupae permitted a 38% reduction in fish oil (i.e., from 13 to 8%); however, fish fed black soldier fly diets low in fish oil had reduced levels of omega-3 fatty acids in their muscle fillets. The findings from this study suggest that either the black soldier fly or the housefly may be a suitable feedstuff for rainbow trout diets.