Fish Offal Recycling by The Black Soldier Fly Produces A Foodstuff High in Omega-3 Fatty Acids

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JOURNAL OF THE Vol. 38, No.

2
WORLD AQUACULTURE SOCIETY June, 2007

Fish Offal Recycling by the Black Soldier Fly Produces


a Foodstuff High in Omega-3 Fatty Acids
SOPHIE ST-HILAIRE1 AND KATIE CRANFILL
Department of Biological Sciences, Idaho State University, Pocatello, Idaho 83209 USA

MARK A. MCGUIRE AND ERIN E. MOSLEY


Department of Animal & Veterinary Science, University of Idaho, Moscow, Idaho 83844 USA

JEFFERY K. TOMBERLIN
Texas A&M University, Texas Cooperative Extension, Stephenville, Texas 76401 USA

LARRY NEWTON
Department of Animal & Dairy Science, University of Georgia, Tifton, Georgia 31794 USA

WENDY SEALEY
Hagerman Fish Culture Experimental Station, University of Idaho,
Hagerman, Idaho 83332 USA

CRAIG SHEPPARD
CEFAS, Weymouth Laboratory, Weymouth, Dorset DT4 8UB UK

STEPHEN IRVING
Department of Entomology, University of Georgia, Tifton, Georgia 31794 USA

Abstract.—The black soldier fly, Hermetia illucens, has fly, Hermetia illucens, has been investigated for
the potential to reduce animal waste on livestock facilities its manure bioconversion capabilities (Sheppard
and produce an animal-grade feedstuff high in protein and et al. 1994, 1998; Newton et al. 2005). It has been
fat. The lipid content of insects is largely dependent on their
diet. Data from this study suggest that black soldier fly estimated that this nonpest fly species can reduce
prepupae incorporate a-linolenic acid (ALA), eicosapen- nitrogen and phosphorus waste by up to 75%,
taenoic acid (EPA), and docosahexaenoic acid (DHA) when and the mass of manure residue by over 50% in
fish offal is included in their diet. Fly larvae were fed three poultry and swine systems (Sheppard et al.
different proportions of fish offal and cow manure diets over 1994, 1998; Newton et al. 2005). Further, the
a 21-d trial. An additional group of larvae were fed 22% fish
offal diet within 24 h of their pupation. Larvae fed fish offal prepupae are approximately 40% protein and
were, on average, 30% lipid, which was 43% more than the 30% fat (Sheppard et al. 1994, 1998; Newton
controls fed cow manure only, and approximately 3% of et al. 2005), which makes for a suitable source
this lipid was omega-3 fatty acids (EPA, DHA, and ALA). of food for animals (Newton et al. 1977; Bondari
Furthermore, this concentration of omega-3 fatty acids was
and Sheppard 1981, 1987).
achieved within 24 h of feeding fish offal. These omega-3
fatty-acid-enhanced prepupae may be a suitable fish meal
In a recent study where rainbow trout, Onco-
and fish oil replacement for carnivorous fish and other rhynchus mykiss, were fed diets containing
animal diets. In addition, they may provide a method of black soldier fly prepupae, it was determined
reducing and recycling fish offal from processing plants. that replacement of 25% of the fish meal and
38% of the fish oil components of a commercial
Manure management is a growing concern in diet (with 40% protein – 67% of which was
intensive livestock facilities. The black soldier derived from fish meal and the other 33% from
plant origin, and 15% lipid – all derived from
1 Corresponding author. fish oil) had no effect on the feed conversion
Ó Copyright by the World Aquaculture Society 2007

309
310 ST-HILAIRE ET AL.

ratio (St-Hilaire et al. 2007). However, the fillets towel, weighted, and frozen for fatty acid an-
of fish fed black soldier fly prepupae were lower alysis. Prepupae were sent frozen to the De-
in omega-3 fatty acids than the controls, possi- partment of Animal & Veterinary Science at
bly because of lower levels of long-chain unsat- University of Idaho, Moscow, Idaho, USA, for
urated fatty acids in their diets. fatty acid analysis.
The lipid content of insects is largely depen-
dant on their diets and stage of development Fatty Acid Analyses
(Stanley-Samuelson and Dadd 1983) and many Prepupae were freeze dried before lipids were
insects have naturally occurring long-chain extracted using chloroform : methanol (2:1)
unsaturated fatty acids (Thompson 1973). The (Clark et al. 1982). Direct methylation of
objective of this study was to determine if the extracted lipids was conducted (Kramer et al.
omega-3 fatty acid content of black soldier fly 1997). The fatty acid methyl esters were ana-
prepupae could be increased by feeding them lyzed on a gas chromatograph (Hewlett-Packard
fish waste from processing plants. 6890 Series with autoinjector) fitted with a flame
ionization detector and a 100 3 0.25 mm, with
Materials and Methods 0.2-mm film capillary column coated with CP-
Approximately 1000 black soldier fly eggs Sil 88 (Chrompack, Middelburg, the Nether-
were collected from an established colony at lands). Initially, the oven temperature was
Texas A&M University Extension service 70 C (for 3 min) and then increased to 175 C
(Stephenville, TX, USA) and sent to Idaho State at a rate of 3 C/min and held for 3 min. Oven
University, Pocatello, Idaho, USA. The eggs temperature was then increased to 185 C at a rate
were hatched and grown on cow manure at room of 1 C/min and held for 20 min, increased to
temperature (;22 C). After 37 d, 50 larvae 215 C at a rate of 3 C/min, and then increased
were counted into 1 of 12 containers and weighed to 230 C at a rate of 10 C/min and held for
(average total weight in containers 4.68 g; 5 min. Response correction factors determined
SE 5 0.141 g and range 3.73–5.42 g). Contain- by the analysis of a butter oil standard with cer-
ers were randomly allocated to four diets: tified values (CRM 164; European Community
manure only, 50/50 mixture of cow manure Bureau of Reference, Brussels, Belgium) were
and fish offal, 25% fish offal mixed with 75% used to quantify fatty acids. Fatty acids were ex-
cow manure, and 10% fish offal mixed with pressed as a weight percentage of total lipid on
90% cow manure. The fish offal included in a dry matter basis.
the larval diets consisted of homogenized heads,
viscera, and some bony structures from rainbow Statistical Analyses
trout processed at a plant in Idaho, USA. The average weight of larvae and prepupae
Larvae were fed 3 d a week. A total of 150 g were compared using an ANOVA. If the
wet weight of food was provided to each con- ANOVA statistic was significant (P , 0.05), then
tainer over a 21-d period. Approximately Tukey tests were used for multiple comparisons.
1 mL of water was sprayed into the containers The total percent lipid and proportion of specific
when the diet was dry (five times during the trial fatty acids of prepupae fed different diets were
period). At the end of the 21-d study, the prepu- compared using the Kruskal–Wallis statistic.
pae were collected, dried with a paper towel, This statistical test was used because the number
counted, weighed, and frozen for future fatty of replicates in each group was low (n 5 3), and
acid analysis. for seven of the 12 fatty acids assessed, the para-
A sample of larvae (n 5 5) from two of the metric test assumption of homoscedasticity was
three control groups (fed cow manure only) violated. The Kruskal–Wallis tests and all
were transferred into two new containers and descriptive statistics were done using MINI-
fed 21 g of material containing 22% fish offal TABÒ Statistical Software (Mintab Inc., State
and 78% cow manure. The prepupae/larvae College, PA, USA). The ANOVA and Tukey
were harvested within 24 h, dried with a paper tests were done using SPSS v.14.0 for Windows
FISH OFFAL RECYCLING BY THE BLACK SOLDIER FLY 311

(SPSS, Inc., Chicago, IL, USA). P values of less 21 d) was 30% lipid, approximately 1% of its
than 0.05 were considered significant. total dry weight was omega-3 fatty acids (Fig. 1).
Greater weight percentages of ALA, EPA, and
Results DHA were also detected in prepupae fed 22% fish
The average weight of the larvae in each of offal for 24 h; however, total lipid was not
the diet treatments at the start of the 21-d trial changed compared to the cow-manure-only con-
was similar (range 0.088–0.096 g) (F3,8 5 0.377, trol so the quantity of omega-3 fatty acids on
P 5 0.772) (Table 1). The final average weight a percent dry weight basis was 0.8% (Fig. 1).
of the prepupae fed cow manure only was
lower than the other diet groups fed a mixture Discussion
of manure and fish offal (F3,8 5 13.29, P 5 Black soldier fly larvae were able to ‘‘recy-
0.002) (Table 1). cle’’ a proportion of the fish oils from processing
There was approximately a 43% increase plant fish offal. Prepupae fed as little as 10% fish
(from 21 to 30%) in total lipid of black soldier offal had approximately 43% more lipid than
flies fed different proportions of fish offal during prepupae fed cow manure without fish offal,
a 21-d period compared to the prepupae fed only and went from negligible amounts of omega-3
cow manure (H 5 9.27, P 5 0.055) (Table 2). fatty acids to approximately 3% of the lipid con-
The percent total lipid was not affected by the sisting of these long-chain unsaturated fatty
proportion of fish offal in the larval diet acids (Table 2). Furthermore, it may be possible
(Table 2). There was no difference between to attain these levels of omega-3 fatty acids in
the percent lipid of prepupae fed fish offal for prepupae by incorporating a small amount of
only 24 h and the control prepupae (Table 2). fish waste in their diet within 24 h of pupation.
The proportion of the omega-3 fatty acids in Currently, much of the rainbow trout fish offal
the prepupae was increased when they were in Idaho is sold for the pet food industry or as
fed fish offal (Table 2). Approximately 3% of compost. This study suggests it could be made
the lipid in the prepupae fed fish offal was into a value-added insect product potentially
omega-3 fatty acids (Table 2). This proportion suitable for animal diets. Black soldier fly raised
of omega-3 fatty acids was similar regardless on poultry manure have been fed to several
of the concentration of fish offal in the diet or commercial species including poultry; catfish,
the length of time the larvae were fed fish offal Ictalurus punctatus; blue tilapia, Oreochromis
(Table 2). Approximately 0.7% of the lipid in aureus; and swine (Newton et al. 1977; Bondari
fish offal fed prepupae was a-linolenic acid and Sheppard 1981, 1987; Newton et al. 2005).
(18:3n3; ALA), 1.7% eicosapentaenoic acid Increasing the omega-3 fatty acid content of
(20:5n3; EPA), and 0.5% docosahexaenoic prepupae should increase the value of this prod-
acid (22:6n3; DHA) when the prepupae were uct as a diet ingredient.
fed any proportion of fish offal for 21 d (Table 2). The growth of prepupae on cow manure was
Given the average prepupae (fed fish offal for slower than what has been reported for poultry

TABLE 1. Average weight (g) of black soldier fly, Hermetia illucens, larvae at the start and prepupae at the end of the
trial (SE).1

Average weight Average weight


of larvae at the start of larvae at the end
Group of the trial (g) of the study (g)
Cow manure only 0.09 (0.003) 0.10 (0.008)a
10% fish offal/90% cow manure 0.10 (0.005) 0.14 (0.003)b
25% fish offal/75% cow manure 0.09 (0.008) 0.16 (0.004)b
50% fish offal/50% cow manure 0.10 (0.006) 0.15 (0.010)b
P value associated with the ANOVA statistic 0.772 0.002
1 Values within columns with a common superscript do not differ (P . 0.05) based on the Tukey multiple comparison test.
312 ST-HILAIRE ET AL.

TABLE 2. Mean 6 SE of selected fatty acid composition of black soldier fly, Hermetia illucens, prepupae fed diets with
varying proportions of fish offal and cow manure. All proportions are expressed as a weight percentage of the total lipid
on a dry matter basis.

Black soldier fly prepupae fed


P value
10% fish offal 25% fish offal 50% fish offal 24 h 22% fish associated
and 90% and 75% and 50% offal and 78% with the Kruskal–
Fatty acid Cow manure cow manure cow manure cow manure cow manure Wallis test
Total lipid – %
of total
dry weight 21.42 ± 0.17 30.38 ± 0.62 28.82 ± 1.46 30.44 ± 1.17 20.28 ± 2.95 0.055
12:0 20.92 ± 1.27 34.10 ± 1.33 41.00 ± 2.01 42.57 ± 0.51 14.72 ± 0.75 0.019
14:0 2.85 ± 0.07 6.46 ± 0.04 6.67 ± 0.16 6.91 ± 0.04 4.51 ± 0.42 0.023
16:0 16.05 ± 0.06 14.30 ± 0.37 12.08 ± 0.53 11.14 ± 0.24 16.50 ± 0.65 0.019
18:0 5.68 ± 0.06 2.35 ± 0.06 1.64 ± 0.09 1.29 ± 0.06 6.22 ± 0.35 0.014
18:1c9 32.11 ± 1.01 16.52 ± 0.34 13.96 ± 0.48 12.28 ± 0.10 27.00 ± 0.65 0.014
18:2n6 4.51 ± 0.56 3.96 ± 0.21 3.22 ± 0.16 3.57 ± 0.09 3.89 ± 0.33 0.060
18:3n3; ALA 0.19 ± 0.01 0.74 ± 0.02 0.71 ± 0.05 0.74 ± 0.03 0.86 ± 0.10 0.091
20:4n6 0.04 ± 0.01 0.20 ± 0.01 0.18 ± 0.01 0.20 ± 0.01 0.19 ± 0.01 0.073
20:5n3; EPA 0.03 ± 0.01 1.76 ± 0.07 1.63 ± 0.05 1.66 ± 0.05 1.43 ± 0.04 0.034
22:5n3 0 0.1 ± 0.003 0.11 ± 0.01 0.14 ± 0.01 0.53 ± 0.04 0.017
22:6n3; DHA 0.006 ± 0.003 0.41 ± 0.01 0.43 ± 0.06 0.59 ± 0.04 1.66 ± 0.01 0.019
Total ALA, EPA,
and DHA 0.23 ± 0.02 2.91 ± 0.11 2.76 ± 0.13 2.99 ± 0.11 3.96 ± 0.05 0.034
ALA 5 a-linolenic acid; EPA 5 eicosapentaenoic acid; DHA 5 docosahexaenoic acid.

or swine manure. It required almost 2 mo for vae. It is also possible that the black soldier fly
eggs to develop into prepupae in this study, does not grow as well on cow manure compared
whereas other researchers report 4–6 wk when to swine or poultry manures. This finding has
larvae are fed poultry manure (Tomberlin et al. been observed by several of the authors indepen-
2002). It is possible that the lower temperature dently of this research (Newton et al. 2005).
used to grow the larvae in this study (i.e., 22 C) The biodegradability of manure has been
contributed to the slower development of the lar- shown to be highly dependent on its lignin

1.2

ALA EPA
1
Percent of total dry weight (%)

DHA Total

0.8

0.6

0.4

0.2

0
Manure only 10% fish offal 25% fish offal 50% fish offal 24 hr fish offal
Diets
FIGURE 1. Percent a-linolenic acid (ALA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) on a total dry
matter basis for prepupae fed diets containing different proportions of fish offal. Error bars indicate the pooled SE.
FISH OFFAL RECYCLING BY THE BLACK SOLDIER FLY 313

content (Stanogias and Pearce 1987), which Kramer, J. K. G., V. Fellner, M. E. R. Dugan,
comes mainly from forage fibre in the diet. F. D. Sauer, M. M. Mossoba, and M. P. Yurawecz.
1997. Evaluating acid and base catalysts in the
Because poultry and swine diets generally con-
methylation of milk and rumen fatty acids with special
tain little forage, it would be expected that their emphasis on conjugated dienes and total trans fatty
feces would be more highly degradable than that acids. Lipids 32:1219–1228.
of ruminants. The lower nutritional value of cow Newton, G. L., C. V. Booram, R. W. Barker, and
manure may explain why the larvae fed mixed O. M. Hale. 1977. Dried Hermatia illucens larvae
diets had higher average weights compared to meal as a supplement for swine. Journal of Animal
prepupae fed cow manure only (Table 1) and Science 44:395–400.
Newton, G. L., D. C. Sheppard, D. W. Watson,
why it required more time to produce prepupae
G. J. Burtle, C. R. Dove, J. K. Tomberlin, and
than previously reported. Analysis of cow E. E. Thelen. 2005. The black soldier fly, Hermetia
manure is under way to further elucidate the illucens, as a manure management/resource recovery
reason for this apparent reduced growth. tool. Symposium on the state of the science of Animal
The lipid content of black soldier fly prepupae Manure and Waste Management, January 5–7, 2005,
can be increased and manipulated to include San Antonio, Texas, USA. Retrieved April 10, 2007,
desirable fatty acids such as ALA, EPA, and from http://www.cals.ncsu.edu/waste_mgmt/natlcenter/
sanantonio/proceedings.htm.
DHA by feeding the larvae waste material from
Sheppard, D. C., G. L. Newton, S. A. Thompson, and
fish processing plants. Our findings indicate an S. Savage. 1994. A value added manure management
increase (from 21 to 30%) in the lipid content system using the black soldier fly. Bioresource Tech-
of prepupae fed fish waste, and more impor- nology 50:275–279.
tantly, substantial enrichment (2.5–3.8% of total Sheppard, D. C., G. L. Newton, S. A. Thompson,
lipid) of omega-3 fatty acids (Table 2). It may J. Davis, G. Gasho, and K. Bramwell. 1998. Using
soldier flies as a manure management tool for volume
therefore be possible to utilize the black soldier
reduction, house fly control and feedstuff production.
fly, which is a nonpest species to reduce animal Page 51 in G. Roland, editor. Sustainable Agriculture
waste and recycle omega-3 fatty acids, while Research and Education, Southern Region, 1998.
producing a high-quality animal-grade foodstuff Annual Report. Sustainable Agriculture Research and
that is a suitable replacement for fish meal and Education, Southern Region, Georgia Station, Griffin,
fish oil in animal diets. Georgia, USA.
Stanley-Samuelson, D. W. and R. H. Dadd. 1983.
Acknowledgments Long-chain polyunsaturated fatty acids: patterns
of occurrence in insects. Insect Biochemistry. 13:
This research was funded by Idaho State 549–558.
University (FRC grant #951). We thank Stanogias, G. B. and G. R. Pearce. 1987. The effects of
W. Chalmers and T. G. Gaylord for their composition on diet digestibility by pigs and on the
editorial comments. biodegradability of the resulting pig faeces. Biological
Wastes 21:101–110.
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