ORIGINAL RESEARCH
Minerals content of extruded fish feeds containing cricket
(Acheta domesticus) and black soldier fly larvae (Hermetia
illucens) fractions
F. G. Irungu . C. M. Mutungi . A. K. Faraj . H. Affognon .
C. Tanga . S. Ekesi . D. Nakimbugwe . K. K. M. Fiaboe
Received: 27 October 2017 / Accepted: 14 February 2018
 The Author(s) 2018. This article is an open access publication
Abstract Animal food sources provide human beings with minerals considerably in adequate quantities. Fish
is an indispensable reliable source of nutrients, as aquaculture is a sector that is fast growing and which
provides 50% of the world’s fish production. However, fish production is hampered by the increasing costs of
feeds due to the ever rising cost of fish meal, an integral component of fish feeds. Substituting fish meal with
cheap, yet highly nutritious ingredients in fish feeds is therefore paramount. This study investigated the effects
of substituting fish meal with adult cricket meal (ACM) and black soldier fly meal (BSFM) on minerals
content of extruded fish feeds, where four levels of substitution (0, 25, 50 and 75%) were used. The effect of
feed moisture content on minerals was also studied where 20 and 30% feed moisture levels were used.
Leaching effects of the pellets were studied as well. The results showed a significant increase (P\ 0.05) in the
levels of phosphorus and potassium as the level of fish meal substitution increased from 0 to 75%. On the other
hand, iron and sodium levels reduced significantly (P\ 0.05) as the level of fish meal substitution increased.
Magnesium content increased with increasing level of substitution with BSFM, but decreased with increasing
level of substitution with ACM. Copper, zinc and manganese were not greatly influenced by levels of fish meal
substitution. Diets that had zero substitution showed higher leaching effect for most minerals than diets that
were substituted with 75% ACM or BSFM. This study found that both ACM and BSFM can be used to
substitute fish meal in fish feeds and obtain adequate mineral profile and low leaching effect.
Keywords Fish meal  Substitution  Cricket  Black soldier fly larvae  Minerals  Extrusion
F. G. Irungu (&)  C. M. Mutungi  A. K. Faraj
Department of Dairy and Food Science and Technology, Egerton University, P. O. Box 536-20115, Egerton, Kenya
e-mail: gichuhofrancis@gmail.com
C. M. Mutungi  C. Tanga  S. Ekesi  K. K. M. Fiaboe
International Centre of Insect Physiology and Ecology, P. O. Box 30772-00100, Nairobi, Kenya
C. M. Mutungi
International Institute of Tropical Agriculture (IITA), Plot NO. 25, Mikocheni Light Industrial Area, Dar es Salaam,
Tanzania
H. Affognon
International Crops Research Institute for the Semi-Arid Tropics, BP 320, Bamako, Mali
D. Nakimbugwe
Department of Food Technology and Nutrition, School of Food Technology, Nutrition and Bio-Engineering, Makerere
University, P. O. Box 7062, Kampala, Uganda
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Int Aquat Res
https://doi.org/10.1007/s40071-018-0191-8
Introduction
Food insecurity is a threat to many nations, especially the developing countries. In fact, 10.9% of the world’s
population (795 million people) is undernourished. This situation is worse in the sub-Saharan Africa where
Middle Africa and East Africa have 41.3 and 31.5% of their population being undernourished, respectively
(FAO 2015). Animal food sources provide protein of high value as well as a variety of micronutrients such as
minerals in adequate quantities (FAO 2012; Murphy and Allen 2003). In addition, nutrients from animal food
sources are more bio-available than most plant sources (Trumpo et al. 2001). Fish is one such source that
provides 17% of animal protein to the world’s population (Halden et al. 2014). Given the forecasted 9 billion
in world population by the year 2050, fish becomes an indispensable reliable source of nutrients as aquaculture
is also fast growing (Msangi et al. 2013; Halden et al. 2014; FAO 2014). Fishmeal, an integral ingredient in
fish feed is becoming extremely expensive due to fluctuations in its production and this has contributed to high
cost of feeds (FAO 2012, 2013, 2014; Njagi et al. 2013). There is thus the need to identify better alternatives to
fishmeal. Insects such as crickets (Acheta domesticus) and black soldier fly (Hermetia illucens) have that
potential (FAO 2013; Bondari and Sheppard 1981; Makkar et al. 2014), due to their high nutritional profile
(Henry et al. 2015; FAO 2010; van Huis 2013), high bio-conversion ratio (Barroso et al. 2014) and their ability
to produce less greenhouse gases and to be reared on less land area (Oonincx et al. 2010).
Traditionally, insects have been processed using different methods. For example, after harvest, mopane
caterpillar is normally sun dried with the aim of achieving higher shelf life (Mutungi et al. 2017). In China,
silkworm pupa, the most widely consumed insect, is normally fried in oil, boiled using water or in some cases
milled into powder (Belluco et al. 2013). Other traditional processing methods of edible insects include sun
drying, roasting, smoking, boiling as well as removal of unpalatable parts (Rumpold et al. 2014). Sun drying is
cheap and easy to carry out. However, it is dependent on weather conditions and therefore is hampered by such
climatic conditions as wet weather, strong winds as well as mist and fogs. The majority of these methods have
far reaching negative impacts. Drying and toasting of termites and grasshoppers have been attributed to
significant decrease in contents of individual vitamins, including pyridoxine, folic acid, ascorbic acid, niacin,
riboflavin, retinol and a-tocopherol, depending on the insect species (Kinyuru et al. 2010). Additionally, the
in vitro digestibility of proteins in tree locust has been shown to decline upon toasting and boiling, as the
tannin and phytate content increased as a result of these treatments. According to Afiukwa and Okereke
(2013), removal of wings as one of the unpalatable insects’ parts reduces the amount of iron that can be
obtained from Trinervitermes germinates (termite)—an edible insect from Nigeria. Thus, although these
methods have been used to process edible insects in the past, they present a situation where their reliability is
questioned (Chakravorty et al. 2014). Extrusion is a modern processing method that can be used to process
insects and insects-based products such as fish feeds. It has the benefits of improving the nutritional value of
end products, destroying undesirable enzymes and anti-nutritional factors (Nikmaram et al. 2015; Alam et al.
2016; Filipovic et al. 2010) and it has also been shown to enhance the apparent absorption of minerals (Razzaq
et al. 2012; Alonso et al. 2001).
Minerals represent a minor proportion in the feeds’ composition. However, they are required in almost
every aspect of animal metabolism (Alonso et al. 2001; FAO 2017). They are classified either as macro
elements, which are needed by the body in large quantities, or micro elements, needed by the body in small
quantities (FAO 2017; Thompson et al. 2005). Macro elements include phosphorus, calcium, potassium,
magnesium, sodium, chlorine and sulfur, while micro elements are composed of copper, zinc, manganese,
iron, cobalt and iodine, among others (FAO 2017; Webster and Lim 2002). Fish requires these elements as
they help in several functions such as transmission of nerve impulses, acid–base balance, as enzyme cofactors
and activators, normal functioning of muscles, osmoregulation and in the formation of skeletal muscles (FAO
2017; Braga et al. 2016; Hassaan et al. 2013; NRC 1993). Fish may obtain some minerals such as calcium,
sodium and potassium readily from the surrounding water environment (FAO 2017; NRC 1993), but cannot
get adequate amounts of phosphorus, zinc, iron and copper from water (Oliva-Teles 2012; NRC 2011) and
thus these must be supplied by the diet through nutritious feeds (Tang et al. 2012). The aim of this experiment
was to study the effects of substituting fish meal with different levels of black soldier fly larvae and cricket
meals on the mineral composition of extruded fish feeds. The effects of moisture content on the mineral profile
of extrudates were also investigated.
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Int Aquat Res
Materials and methods
Research site
Extrusion of feeds was done using a small-scale single screw extruder at Bidii Fish Farmers, Luanda-Vihiga
County, Kenya. Mineral analyses were carried out at Kenya Agricultural and Livestock Research Organization
(KALRO), Njoro, Kenya.
Materials
Maize germ, sunflower cake, dried cassava chunks, wheat pollard and dried freshwater shrimps were pur-
chased from a local vendor in Luanda town, Vihiga County, Kenya. Blanched and sun-dried adult house
crickets (Acheta domesticus L.) were purchased from farmers in Homa Bay County, Kenya, while blanched
and sun-dried black soldier fly larvae (Hermetia illucens L.) were obtained from Sanergy Limited, Nairobi,
Kenya, a commercial insect rearing farm. Each ingredient was then ground separately into fine meal using a
hammermill (Model 4, ARTHUR H. THOMAS, Philadelphia, PA, USA) and finally passed through a 1.0 mm
aperture sieve.
Experimental design
A 2 9 4 9 2 factorial arrangement in a completely randomized design was used. The factors investigated
were insect type (two levels; black soldier fly larvae and adult cricket), level of freshwater shrimp meal
(FWSM) protein substitution with black soldier fly larvae meal (BSFM) or adult cricket meal (ACM) (four
levels: 0, 25, 50 and 75%), and feed moisture content (two levels: 20 and 30% on wet weight basis). The
experiment was replicated three times.
Feed formulation
The quantities of the ingredients required to formulate iso-proteinaceous diets (26% protein; 5 kg formulation)
and the amount of water needed to achieve a required moisture content (on wet weight basis) were calculated
using Microsoft Excel function on Windows 2007 and weighed using an electronic digital weighing scale
(Model no.: 7765, Ashton Meyers, China), into a 20-L bucket. These were mixed manually for 2 min and then
transferred to a multi-vane paddle mixer (Model: MX-25, Unitech, New Delhi, India) for further mixing for
2 min. The control diet and the insect-based formulations are shown in Table 1.
Extrusion process
A single screw extruder (Model: DOLLY, Unitech, New Delhi, India), with a screw operating at a speed of
200 rpm was used. The extruder was equipped with a pre-conditioning chamber where blended ingredients
were introduced through a manual hopper at a feed rate of 1 kg/min and preheated with steam at an inlet
pressure of 4 bars for approximately 2 min. The mixture was then channeled into the extrusion jacket that
housed a single screw with a barrel length and diameter of 55 and 6 cm, respectively. The extruder was set to
operate at 120 C and fitted with a die that had a diameter of 2 mm at the exit. Each extruded batch was
collected into separate 20 L bucket and then dried in a solar tent for about 4 h to constant weight. About 500 g
of the dried pellets were taken in duplicate and packed into zip-lock bags, which were placed in cool and dry
wooden locker boxes for further analysis.
Minerals analyses
Freshwater shrimps, cricket, black soldier fly larvae and extruded sample diets were milled using an oscillating
mill (Model: MM400; S/N: 129251116; Retsch, Germany) and weighed using an electronic weighing balance
(Model: ABS 220-4; S/N: WB1210455; KERN & SOHN GmbH, Germany). Mineral contents were then
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Int Aquat Res
determined by atomic absorption spectrometry in an atomic absorption spectrophotometer (Model: AA-6300;
S/N: A305243009165A; Shimadzu, Japan) after digestion in sulfuric acid and selenium powder. Calcium,
potassium, magnesium, sodium, copper, zinc, manganese and iron were measured at wavelengths of 422.7,
766.5, 285.2, 589.0, 324.8, 213.9, 279.5 and 248.3 nm, respectively. Phosphorus was determined using a UV–
visible spectrophotometer (Model; UV-1700; S/N: A11024302429LP; Shimadzu, Japan) and measured
through a wavelength of 880 nm.
Leaching activity
For each measurement, three replicates were performed. About 5 g of sample was weighed and introduced
into a 250 mL measuring cylinder containing 200 mL distilled water. Aliquots (5 mL) of the supernatant were
drawn after 4, 8, 24 and 48 h and sodium azide added at a rate of 0.02% into the tubes containing the aliquots.
Mineral analyses were then determined as outlined above.
Statistical analysis
Analysis was done using general linear model procedure (PROC GLM) of the Statistical Analysis System
(SAS) software version 9.1.3 (SAS Institute Inc., USA) for analysis of variance (ANOVA). Means were
separated using Tukey’s HSD (honestly significant difference) test at P\ 0.05 level of significance.
Results
The mineral profile of freshwater shrimp meal, adult cricket meal and black soldier fly meal
Phosphorus and potassium were significantly (P\ 0.05) higher in BSFM than in FWSM, though the two
elements did not show significant (P\ 0.05) difference between BSFM and ACM (Table 2). Calcium was
significantly (P\ 0.05) higher in FWSM than both in ACM and BSFM. Magnesium was significantly
(P\ 0.05) higher in BSFM than in FWSM and ACM, while FWSM had significantly (P\ 0.05) higher
magnesium than ACM (Table 2). Sodium, copper and zinc were higher (P\ 0.05) in both BSFM and ACM
than in FWSM. Adult cricket meal showed significantly (P\ 0.05) higher amounts of manganese than FWSM
and BSFM. Iron was higher (P\ 0.05) in ACM and FWSM than in BSFM (Table 2).
Table 1 Inclusion levels of insects’ meals in freshwater shrimp meal substitution
Ingredient Control Inclusion level of insects (%)
BSFM25 BSFM50 BSFM75 ACM25 ACM50 ACM75
Maize germ 19 18.5 18.1 17.6 19.2 19.4 19.6
Sunflower cake 19 18.5 18.1 17.6 19.2 19.4 19.6
Cassava flour 5 4.9 4.8 4.6 5 5.1 5.2
Wheat pollard 28.5 27.8 27.1 26.5 28.8 29.1 29.4
FSWM 28.5 20.9 13.6 6.6 21.6 14.5 7.3
BSFM – 9.5 18.4 27.1 – – –
ACM – – – – 6.3 12.5 19.1
FWSM freshwater shrimp meal, BSFM black soldier fly meal, ACM adult cricket meal, BSFM25 black soldier fly meal substituting
25% of the protein supplied by FWSM in the control, BSFM50 black soldier fly meal substituting 50% of the protein supplied by
FWSM in the control, BSFM75 black soldier fly meal substituting 75% of the protein supplied by FWSM in the control, ACM25
adult cricket meal substituting 25% of the protein supplied by FWSM in the control, ACM50 adult cricket meal substituting 50%
of the protein supplied by FWSM in the control, ACM75 adult cricket meal substituting 75% of the protein supplied by FWSM in
the control
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Int Aquat Res
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123
Int Aquat Res
Macro minerals as influenced by different diets extruded at various feed moisture contents
The level of phosphorus in control diets was significantly (P\ 0.05) lower than in all the insect-based diets
(Table 3). As the level of insect substitution increased, so did the level of phosphorus. However, for each level
of insect substitution, BSFM-based diets recorded higher values of phosphorus than ACM diets. Moisture
content had a significant (P\ 0.05) effect on phosphorus only for the BSFM50 and BSFM75 diets. The
highest level of phosphorus was recorded for the BSFM75 diet that had feed moisture content of 30%.
The control diet that was extruded with feed moisture content of 20% gave the highest amounts of calcium
(Table 3). This level, however, did not show significant (P\ 0.05) difference with the BSFM25 and ACM25
diets that were produced at 20% feed moisture content, or the control diet that had 30% feed moisture content.
The increase in the level of insect substitution led to a corresponding decrease in calcium levels. However,
BSFM-based diets had higher calcium levels than the corresponding ACM diets (Table 3). The moisture
content was also found to have a significant (P\ 0.05) influence on calcium, where for each formulation
calcium was slightly higher for the extrudates that had 20% feed moisture content than those that had a feed
moisture content of 30%.
The level of potassium appeared to increase with increasing level of fish meal substitution for each insect-
based diet (Table 3). This increase was significant (P\ 0.05), apart from the ACM25 diet that did not show
significant (P\ 0.05) difference with the control diet. Another peculiar observation was that for each diet, the
moisture content showed a significant (P\ 0.05) influence on potassium, where increasing the amount of feed
moisture content from 20 to 30% resulted in a corresponding slight increase in the level of potassium
(Table 3).
The amount of available magnesium seemed to increase as the level of fish meal substitution with BSFM
increased (Table 3). On the contrary, increasing the level of fish meal substitution with ACM led to a slight
decrease in the amount of magnesium. In addition, increasing the level of feed moisture content resulted in
Table 3 Effects of different levels of freshwater shrimp meal substitution with different insect species extruded at different feed
moisture contents on phosphorus (P), calcium (Ca), potassium (K), magnesium (Mg) and sodium (Na) of the extrudates
Diet MC (%) P (ppm) Ca (ppm) K (ppm) Mg (ppm) Na (ppm)
Control 20 625.9 ± 19.9e 15,063.8 ± 300.6a 6220.8 ± 0.7e 3287.6 ± 4.5e 1268.3 ± 9.2a
30 649.4 ± 13.5e 14,476.2 ± 114.6ab 6229.4 ± 2.4e 3318.9 ± 5.8de 1157.8 ± 31.5bc
BSFM25 20 712.6 ± 26.6d 14,696.9 ± 420.8ab 6335.4 ± 0.59d 3436.1 ± 31.4abcde 1223.9 ± 7.0ab
30 735.9 ± 39.8d 10,752.5 ± 37.8cd 6341.8 ± 3.8c 3519.1 ± 4.4ab 1107.6 ± 19.7c
BSFM50 20 810.6 ± 10.1b 13,077.1 ± 1412.7abc 6359.5 ± 8.55b 3451.9 ± 13.4abcd 991.9 ± 44.4d
30 789.3 ± 6.7c 10,386.2 ± 370cd 6370.5 ± 10.4b 3467.6 ± 10abcd 804.7 ± 7.4ef
BSFM75 20 804.2 ± 14.9b 9646.2 ± 1053.9cde 6362.5 ± 2.3b 3491.6 ± 60.9abc 492.1 ± 16.4g
30 840.9 ± 4.9a 8855.8 ± 218.6de 6385.9 ± 5.3a 3597.5 ± 49.1a 442.9 ± 5.3g
ACM25 20 718.2 ± 2.3d 14,613.2 ± 392.4ab 6226.3 ± 3.6e 3450.3 ± 42.4abcd 1145.7 ± 18.4bc
30 715.9 ± 23.3d 12,824.8 ± 409.3bc 6243.1 ± 6.7e 3383.8 ± 14.2bcde 1049.6 ± 10.1d
ACM50 20 749.4 ± 6.5 cd 8911.8 ± 1519.3de 6359.7 ± 9.2b 2956.6 ± 32.6f 812.4 ± 33.6ef
30 769.9 ± 30.7bc 4326.1 ± 39.2f 6383.5 ± 8.4a 2837.6 ± 38.4f 717.9 ± 11.6f
ACM75 20 782.1 ± 12.7bc 6439.6 ± 392.4ef 6385.3 ± 0.6a 3334.8 ± 12.02cde 878.2 ± 4.8e
30 767.8 ± 21.6bc 4074.9 ± 357.7f 6389.5 ± 3.3a 2934.4 ± 17.8f 766.09 ± 18.47f
Extrusion was done at a barrel temperature of 120 C and feed exited through a 2 mm die
For each component, means followed by the same superscript letters along the same column are not significantly different at
P\ 0.05
MC moisture content, P phosphorus, Ca calcium, K potassium, Mg magnesium, Na sodium, Control 0% insect substitution of
FWSM, BSFM25 black soldier fly meal substituting 25% of the protein supplied by FWSM in the control, BSFM50 black soldier
fly meal substituting 50% of the protein supplied by FWSM in the control, BSFM75 black soldier fly meal substituting 75% of the
protein supplied by FWSM in the control, ACM25 adult cricket meal substituting 25% of the protein supplied by FWSM in the
control, ACM50 adult cricket meal substituting 50% of the protein supplied by FWSM in the control, ACM75 adult cricket meal
substituting 75% of the protein supplied by FWSM in control
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Int Aquat Res
higher amounts of magnesium for the control and BSFM diets, but resulted in lower levels of magnesium for
the ACM diets (Table 3).
Increasing the level of fish meal substitution with insect meal beyond 25% resulted in lower levels of
sodium, where BSFM50, BSFM75, ACM25, ACM50 and ACM75 diets gave significant (P\ 0.05) lower
amount of sodium than the control diet (Table 3). Moreover, increasing the amount of feed moisture content
from 20 to 30% resulted in a significant (P\ 0.05) reduction in the amount of sodium (Table 3) for all the
diets, apart from BSFM75 whose reduction was not significant (P\ 0.05).
Micro minerals as influenced by different diets extruded at various feed moisture contents
Copper levels in control diets did not show significant (P\ 0.05) difference compared with BSFM75, ACM25
and ACM50 diets that were extruded with 30% feed moisture content (Table 4). The ACM75 diet extruded at
both 20 and 30% feed moisture gave the highest values of copper that significantly (P\ 0.05) differed from
the other formulations. Moisture content showed significant (P\ 0.05) influence on the level of copper, in
that, for each diet, copper levels increased with increasing moisture content (Table 4).
The control diet that had 20% feed moisture content did not have significant (P\ 0.05) difference com-
pared with BSFM25 (20% MC), BSFM50 (20% MC), BSFM75 (30% MC), ACM25 (30% MC) and ACM50
(both 20 and 30% MC) in amount of zinc (Table 4). Similarly, the control diet that had 30% feed moisture
content did not show significant (P\ 0.05) difference in amount of zinc, compared with BSFM50 and
ACM75 diets that were also extruded at 30% feed moisture content as well as BSFM75 that had 20% feed
moisture content. ACM75 diet with 20% feed moisture content gave the highest level of zinc that had
significant (P\ 0.05) difference with all other formulations.
For BSFM diets, there was no definite trend on how different levels of substitution as well as moisture
content influenced manganese (Table 4). However, ACM diets showed slight increase in the levels of man-
ganese as feed moisture content was increased from 20 to 30%. In addition, ACM75 diets gave the highest
Table 4 Effects of different levels of freshwater shrimp meal substitution with different insect species extruded at different feed
moisture contents on copper (Cu), zinc (Zn), manganese (Mn) and iron (Fe) of the extrudates
Diet MC (%) Cu (ppm) Zn (ppm) Mn (ppm) Fe (ppm)
Control 20 83.7 ± 0.4b 158.1 ± 1.3efg 14.9 ± 0.1cd 356.9 ± 1.6cd
30 89.9 ± 1.5b 181.2 ± 4.3b 10.1 ± 0.2ghi 376.7 ± 2.2cd
BSFM25 20 12.5 ± 1.2d 159.5 ± 1.6efg 12.1 ± 0.8efgh 347.4 ± 30.45d
30 16.8 ± 2.7d 145.8 ± 0.5hi 13.8 ± 0.7cde 355.5 ± 11.2d
BSFM50 20 19.4 ± 0.1d 168.3 ± 1cde 18.3 ± 0.3a 271.6 ± 6.4e
30 52.8 ± 0.5c 177.4 ± 1.2bc 15.6 ± 0.9bc 309.7 ± 15.3d
BSFM75 20 44.8 ± 0.0c 171.4 ± 2.8bcd 15.6 ± 0.3bc 207.8 ± 11.9f
30 73.1 ± 5.8b 161.9 ± 3.2def 12.4 ± 0.5efg 255.5 ± 11.2e
ACM25 20 50.9 ± 8.8c 143.1 ± 2.7i 9.9 ± 0.3hi 429.2 ± 5.3b
30 75.1 ± 3.4b 155.3 ± 0.9fgh 12.8 ± 0.2def 469.6 ± 5.9ab
ACM50 20 43.5 ± 4.2c 153.5 ± 1.5fghi 10.6 ± 0.0fghi 467.2 ± 3.2ab
30 75.7 ± 0.0b 148.7 ± 0.8ghi 12.9 ± 0.0def 492.2 ± 6.4a
ACM75 20 152.3 ± 3.8a 199.4 ± 1.2a 17.8 ± 0.2ab 502.4 ± 1.7a
30 170.8 ± 5.6a 186.1 ± 2.5b 18.3 ± 0.3a 521.4 ± 8.2a
Extrusion was done at a barrel temperature of 120 C and feed exited through a 2 mm die
For each component, means followed by the same superscript letters along the same column are not significantly different at
P\ 0.05
MC moisture content, Cu copper, Zn zinc, Mn manganese, Fe iron, Control 0% insect substitution of FWSM, BSFM25 black
soldier fly meal substituting 25% of the protein supplied by FWSM in the control, BSFM50 black soldier fly meal substituting
50% of the protein supplied by FWSM in the control, BSFM75 black soldier fly meal substituting 75% of the protein supplied by
FWSM in the control, ACM25 adult cricket meal substituting 25% of the protein supplied by FWSM in the control, ACM50 adult
cricket meal substituting 50% of the protein supplied by FWSM in the control, ACM75 adult cricket meal substituting 75% of the
protein supplied by FWSM in the control
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values of manganese that did not differ significantly (P\ 0.05) with BSFM50 diets as well as the BSFM75
diet that were extruded at 20% feed moisture content (Table 4).
An increase in level of fish meal substitution with BSFM resulted in a decrease in final iron content, where
BSFM75 diets had significantly (P\ 0.05) lower levels of iron than the control (Table 4). On the other hand,
substitution with ACM resulted in increased levels of iron as the level of substitution increased with all the
ACM diets giving significantly (P\ 0.05) higher levels of iron than the control and BSFM diets. It was also
noted that increasing feed moisture content gave a corresponding increase in the amount of iron for all the
diets, though this increase was only significant (P\ 0.05) for the BSFM50 and BSFM75 diets (Table 4).
Leaching activity
Leaching activity was determined on pellets processed from the control formulation and insect meal con-
taining blends at 75% substitution (BSFM75 and ACM75) and 30% moisture content, because the three
exhibited relatively good mineral profile and have also shown better physico-chemical properties in com-
parison to other treatments (Irungu et al. 2018). Figure 1 shows the leaching activity of minerals that were
studied over a period of 48 h. Phosphorus, calcium, potassium, sodium and manganese were highly leached in
the control diet (as shown in Fig. 1 with asterisks), where, during the period studied, the control showed
significantly (P\ 0.05) higher leaching effect as compared to the ACM75 and BSFM75 diets. The leaching of
magnesium and zinc was significantly (P\ 0.05) higher with the ACM75 diets than with BSFM75 and
control diets throughout the 48 h study period. At 4 h, BSFM75 had significantly (P\ 0.05) lower leached
Fig. 1 Leaching activity of minerals (P phosphorus, Ca calcium, K potassium, Mg magnesium, Na sodium, Cu copper, Zn zinc,
Mn manganese, Fe iron) in water introduced with pellets extruded from the control blend (round dotted line), black soldier fly
larvae meal-containing blend (75% substitution; BSFM75) (solid line) and adult cricket meal-containing blend (75% substitution;
ACM75) (square-dotted line) adjusted to 30% moisture content. Parameters with an asterisk show that the control diet gave
significant (P\ 0.05) higher leaching effect than ACM75 and BSFM75 diets
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copper levels than ACM75 and the control, both of which were not significant at the time. However, at 48 h,
all the three diets had no significant (P\ 0.05) difference in the amount of leached copper. At 4, 8 and 24 h,
BSFM75 had significantly (P\ 0.05) higher amounts of leached iron levels than the control and ACM75
diets. This scenario changed at 48 h where BSFM75 showed significantly (P\ 0.05) low amounts of leached
iron than the control and ACM75 diets, both of which were not significant (P\ 0.05). Another peculiar
observation is that while it is expected for the level of leached minerals to increase as time progresses,
BSFM75 showed a decreasing trend from 24 to 48 h with regard to copper, zinc and iron elements. The
control also showed the same behavior with zinc and copper, while ACM75 only showed a decreased behavior
with copper.
Discussion
The fact that ACM and BSFM were higher in the majority of minerals than FWSM indicates that the two
insects are good sources of minerals and that the two are potential substitutes of FWSM in fish feeds.
Phosphorus and calcium are important minerals required by the fish for healthy bone formation as well as in
enhancing the growth performance of fish (FAO 2016; Braga et al. 2016). The two have an antagonistic effect
where an inadequate supply of one element affects the availability of the other due to the formation of the
calcium–phosphorus complex (Chavez-Sanchez et al. 2000); therefore, both are discussed together. The high
values of phosphorus recorded in BSFM-based diets can be attributed to the fact that BSFM had the highest
amounts of phosphorus in comparison to ACM and FWSM (Table 2). Newton et al. (1977) and Barker et al.
(1998) have also shown that BSFM has higher calcium and phosphorus than ACM. Likewise, the decrease in
calcium amounts as the level of substitution increased is attributed to the high values of calcium that are found
in FWSM in comparison to BSFM and ACM (Table 2). The low levels of calcium as the feed moisture content
was increased to 30% could be due to the formation of solid bridge complexes (Tumuluru et al. 2011) that
hindered the availability of the element. It could also be due to the fact that calcium is highly soluble in water
(Nielsen 2010) and thus a lot of it could have been solubilized in water and leached during the extrusion
process. On the other hand, phosphorus has poor solubility in water and this could explain why feed moisture
content did not have an influence on the amount of available phosphorus. Unlike calcium, phosphorus must be
supplied by the feed because fish cannot get it readily from the surrounding water environment (Tessenderlo
2005; Tang et al. 2012). As such, BSFM- and ACM-based diets are good sources of phosphorus, as both
resulted in higher levels of phosphorus than the control (100% freshwater shrimps) diet. However, none of the
study diets resulted in minimum requirements for phosphorus for tilapia (Oreochromis Niloticus [L]) and
catfish (Clarias gariepinus [Burchell]), which is 5000 ppm and 4500 ppm, respectively (FDKS 2010; FAO
2017), and thus there is need to supplement the feeds with an inorganic source such as dicalcium phosphate so
as to improve feed utilization and growth performance. Since calcium and phosphorus have an antagonist
effect (Hassaan et al. 2013; FAO 2016), the Ca/P ratio of these diets on growth and development of fish need
to be studied.
Potassium is essential in the growth and development of fish, as it regulates acid base balance, intracellular
osmotic pressure and is also required for protein and glycogen synthesis (FAO 2017; NRC 1993). The increase
in potassium as the level of substitution increased is due to the high potassium levels that are found in both
ACM and BSFM in comparison to FWSM (Table 2). The fact that the moisture content influenced potassium
levels shows that extrusion has an influence on this element, which could be due to chemical alteration (Singh
et al. 2007) and destruction of polyphenols (Alonso et al. 2001) through extrusion at high feed moisture
content, which allows phosphorus to become bio-available. Razzaq et al. (2012) also found an increase in
potassium amounts of maize extrudates as moisture content was increased. The minimum potassium
requirements for tilapia and catfish are 2100–3300 and 2600 ppm, respectively, and thus all our study diets
meet these requirements.
Magnesium is required by fish, as it is an essential cartilage and bone component and also stimulates muscle
contraction (Jahnen-Dechent and Ketteler 2012; FAO 2017). The decrease in the amount of magnesium as
FWSM was substituted with BSFM is due to the higher magnesium content that is found in BSFM than in
FWSM (Table 2). Likewise, ACM has lower magnesium content than FWSM (Table 2), the reason why diets
substituted with ACM had lower magnesium content than the control diet. The fiber in ACM could have been
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more susceptible to restructuring due to the extrusion process to an extent of promoting chelating effects that
could have rendered magnesium unextractable, and thus the low magnesium content in ACM diets (Cheftel
1986). According to FAO (2017), the minimum magnesium requirements for tilapia and catfish are 600–800
and 400 ppm, respectively, and all our study diets exceeded these levels. Thus, both BSFM and ACM can be
used to substitute FWSM in fish feed and satisfy magnesium requirements for both tilapia and catfish, given
that fish does not meet all its magnesium requirements from the surrounding water and feeds must supply the
demand (FAO 2017).
Fish need sodium for maintenance of acid base balance and for regulation of osmotic pressure (FAO 2017;
Webster and Lim 2002). The sodium in BSFM and ACM may not be readily available as in FWSM, probably
due to differences in their structural formation, and this could explain why substituting FWSM with BSFM
and ACM resulted in low amounts of sodium. Extrusion at high temperature and high moisture content may
have led to the formation of phenolic complexes that changed the chemical structure of the compounds, thus
rendering sodium unextractable (Alonso et al. 2001). In addition, high feed moisture content may have
lowered the glass transition temperature, leading to the formation of solid bridges (Tumuluru 2014) that
resulted in dense products that made sodium unavailable. There is little information on the minimum sodium
requirements for both tilapia and catfish and thus it is impossible to conclude whether our study diets
(especially insect-based diets) can successfully substitute fish meal and meet the sodium demand for these
fishes.
Copper is directly involved in enzymes activity such as dopamine hydroxylase and cytochrome oxidase
(Watanabe et al. 1997) and also acts as catalyst for some enzymes (Camire et al. 1990). The higher values of
copper in the ACM75 diet than BSFM and control diets is due to the higher copper amounts that were found in
ACM in comparison to BSFM and FWSM (Table 2). The increase in copper as feed moisture content
increased could be due to the ability of water to increase the contact area of feed particles through van der
Waals forces (Tumuluru 2014) and thus increasing the availability of copper. In addition, water used in
extrusion could have had traces of copper, which led to more amount of the element as moisture content was
increased to 30%. Wheat, one of the ingredients used, has also been shown to influence copper levels (Singh
et al. 2007). All the study diets met the minimum requirements for copper in tilapia (6 ppm), as outlined by
KEBS standards (FDKS 2010), as well as the minimum requirements for catfish (5 ppm), as specified by FAO
(2017). Thus, the ACM75 diet can be used to substitute FWSM and still obtain the same or higher values of
copper.
Zinc in fish is involved in many metabolic pathways, serves as a specific cofactor for various enzymes and
has also been shown to assist in healing of wounds (Watanabe et al. 1997; FAO 2017). The KEBS minimum
requirements for tilapia ranges between 50 and 100 ppm depending on the stage of fish that is being targeted
(FDKS 2010), while the minimum requirement for catfish is 20 ppm (FAO 2017). The fact that all the study
formulations were between 100 and 200 ppm and that the control diet did not differ from BSFM50 and
ACM75 demonstrate that BSFM and ACM can be used to substitute FWSM up to 50 and 75%, respectively,
with regard to zinc. The extrusion process has little effect on zinc composition, as the moisture content did not
show significant influence on its content. Other studies have also documented the non-significant influence of
extrusion on zinc and its bio-availability (Guy 2001; Kang and Chenoweth 2000).
Manganese is required in fish for normal brain functioning as well as for the metabolism of carbohydrates
and lipids (Watanabe et al. 1997). The minimum requirements for manganese in feeds intended for tilapia and
catfish are 12 and 2.4 ppm, respectively (FAO 2017). Findings from our study indicate that BSFM50 and
ACM75 are best suited for feeding tilapia, as they contain more than 12 ppm of manganese. However, all the
formulations met the minimum requirements for manganese that is required by catfish. Manganese is one of
the elements that is least affected by the extrusion process and its parameters (Razzaq et al. 2012; Singh et al.
2007), partly due to its electronic configuration that lenders it less susceptible to the formation of chelates
(Alonso et al. 2001). This explains why feed moisture content did not influence the manganese content of the
final products.
Iron is necessary for hemoglobin and myoglobin pigments (FAO 2017) and is actively involved in oxi-
dation/reduction reactions (Watanabe et al. 1997). The decrease in iron content as the level of FWSM
substitution with BSFM increased is attributed to the low iron content that is found in BSFM in comparison to
FWSM (Table 3). Similarly, the corresponding increase in iron content as FWSM is substituted with ACM is
due to the higher iron content in ACM than in FWSM (Table 3). Other researchers have also shown that ACM
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has higher iron content than BSFM (Makkar et al. 2014; Finke 2002; Barker et al. 1998). It should be noted
that all the formulations exceeded the minimum iron requirements for tilapia and catfish (60 and 30 ppm,
respectively) (FAO 2017; FDKS 2010). The extrusion process influenced the amount of iron in the final
products where, for each formulation, the 30% feed moisture content resulted in feeds having higher iron
content. This could be attributed to the fact that moisture and high temperature of the extrusion (120 C)
increased the abrasion of the extruder barrel, screw and the die, thereby increasing the final iron content.
Similar phenomena have been reported by others (Razzaq et al. 2012; Guy 2001; Alonso et al. 2001; Camire
et al. 1990).
Leaching activity
Leaching activity is determined by water stability of feeds, where pellets with low water stability exhibit
higher leaching effect (Saalah et al. 2010; Ayadi et al. 2011). Irungu et al. (2018) had reported that at 30%
moisture content, ACM75- and BSFM75-based pellets had higher water stability than fish feeds that had 100%
FWSM. This explains why the control diet had higher leaching effect for most of minerals than the ACM75
and BSFM75 diets. Our findings are in agreement with those of Haghbayan and Mehrgan (2015) and Hardy
(2002), who reported that fish meal in fish feed increased the nutrient load in wastewater and thus contributed
to higher leaching effect. Phosphorus and sodium leaching leads to eutrophication and algal blooms (Jia et al.
2015; Xiang and Zhou 2011; Saalah et al. 2010), while lack of adequate potassium affects nerve and muscle
formation in fish (Wurts 1993) and thus there is need to substitute fish meal with either ACM75 or BSFM75
meals, as the two lead to low leaching of phosphorus, sodium and potassium as compared to the control. In
addition, fish do not get phosphorus readily from the water environment (Tang et al. 2012), and thus feeds that
have higher phosphorus leaching activity contribute to phosphorus deficiency in fish. Calcium and magnesium
leaching do not pose a serious challenge, as both contribute to water hardness which is important for the
growth of fish. For example, relatively high amounts of free calcium ions in water reduce the loss of sodium
and potassium salts from the body of fish (Wurts 1993). However, high concentration of hard water may
increase the susceptibility of fish to columnaris disease (Avant 2015). The decreasing copper, zinc and iron
leached levels in the BSFM75 diets and copper and zinc in the ACM75 and control diets, respectively, could
be due to formation of complexes by the macro minerals rendering these micro elements unavailable with
time.
Conclusion
Both adult cricket meal and black soldier fly larvae meal can be used to substitute freshwater shrimp meal up
to 75% in fish feeds and supply both tilapia and catfish with adequate quantities of minerals such as potassium.
Further studies should investigate the bio-availability of minerals for fish from these diets.
Acknowledgements This work was supported by the ‘INSFEED—Insect Feed for Poultry and Fish Production in Kenya and
Uganda’ project (Cultivate Africa Grant no.: 107839-001), co-funded by the International Development Research Centre, Canada
(IDRC) and Australia Centre for International Agricultural Research (ACIAR).
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of interest.
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided
you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if
changes were made.
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