REVIEW ARTICLE
Tiroesele and Moreki, IJAVMS, Vol. 6, Issue 5, 2012: 368-376
DOI: 10.5455/ijavms.174
Termites and Earthworms as Potential Alternative Sources of Protein for
Poultry
Bamphitlhi Tiroesele and John Cassius Moreki*
Department of Crop Science and Production, Botswana College of Agriculture, Private Bag 0027,
Gaborone, Botswana
*Corresponding author’s e-mail: [email protected]
Rec.Date: Aug 23, 2012 11:05
Accept Date: Sep 10, 2012 23:34
Abstract
This study set out to review the nutritional composition of termites and earthworms and their
potential value as alternative sources of animal protein in poultry diets. It has been demonstrated that
termites and earthworms have high nutritional value and that they may be an important source of
protein, carbohydrate, fats, vitamins and minerals. In Botswana, feed costs account for over 70% of
the total production costs in commercial poultry production, as nearly all the ingredients used in
manufacturing feeds are imported. This makes the prospect of utilizing insects which are available in
nature for most part of the year as alternative sources of proteins feasible. Nutritionally, it has been
shown that termites and earthworms compare favourably with fish meal, which is the main animal
protein source in poultry diets. Based on the high nutritive value of termites and earthworms, it seems
that there is need to carry out extensive research on their production in order to enable their use in
smallholder poultry production.
Keywords: Earthworms, fish meal, nutrition, poultry, smallholder poultry production, termites
Introduction
At present human population stands at 6.4 billion. It is estimated that the world’s human
population will be 8.1 billion in 2030 and 9 billion in 2050. The greatest increase will occur in
developing countries 42. This increase will lead to the animal protein requirements and demand also
increasing. Therefore, there is a need to exploit not only the known unconventional feed ingredients
but also to determine and introduce new and lesser known plants and animal feed resources. Abd
Rahman Jabir et al 1 stated that insect nowadays has become more promising alternatives protein
source due to the low success in fish meal replacement by animal or plant origins.
Insects make up the majority of the world’s biodiversity and dominate tropical ecosystems in
terms of species richness, biomass and provision of ecosystem services 53. Hundreds of insect species
have been used as human food with some of the more important groups including grasshopper,
caterpillars, beetle grubs and sometimes adults, winged termites (some of which are very large in the
tropics), bee, wasp and ant brood (larvae and pupae), winged ants, cicadas, and a variety of aquatic
insects 7. According to Bernard and Allen 8, protein concentrations in invertebrate species range from
40 to 70% on a dry matter basis (DMB).
ALTERNATIVE SOURCES OF PROTEIN FOR POULTRY
Feed is the most important input for poultry production in terms of production costs. Feed
costs for intensive boiler or layer production account for about 70% of total production costs 50, 24.
Therefore, the availability of high-quality, low-cost feed is a crucial prerequisite for poultry
production 24. Chadd 10 stated that globally, relatively few protein and energy ingredients are used in
the manufacture of poultry feed with a significant reliance on soybean and traditional cereal grains to
achieve nutrient supply and balance. According to Teguia and Beynen 50, the major ingredients of
poultry feeds are maize and imported protein concentrates based on soybean concentrate, fish and/or
animal meals. Presently, the protein sources such as fishmeal are very expensive, especially for
smallholder farmers. As a result, the demand for low cost poultry feed is high, due to the rising cost
and limited supply of commercial feeds 31. Gope and Prasad 20 mentioned that insects represent the
cheapest source of animal protein.
Insects are believed to have a higher proportion of protein and fat than beef and fish with a
high energy value. Depending on the species, caterpillars are rich in minerals such as potassium,
calcium, magnesium, zinc, phosphorus and iron, as well as, various vitamins 47. For example,
mophane worms [Imbrasia belina (Westwood)] have a higher protein, fat, carbohydrate and mineral
content than beef and chicken 29, 4. According to Anand et al 5, the protein content of acridids ranges
from 60 to 66%, indicating that the protein content of acridids is higher than that of soybean meal
(48%) and fish meal (50 to 55%). Hassan et al 21 fed 0%, 50% and 100% grasshopper meal to broiler
chickens and reported that it was capable of replacing significant quantities of fish meal in broiler
diets. In addition, Finke et al 19 fed Mormon crickets (Anabrus simplex Haldeman) diet to broiler
chicks and found that it compared favourably with a corn-soybean meal diet with no significant
differences in weight gain or feed/gain ratios. Furthermore, Fashina-Bombata and Balogun 18 and
Ajani et al 3 fed fly maggot meal to Nile tilapia (O. niloticus) and found that fly maggot was capable
of replacing fishmeal up to 100%. The findings of previous investigations showed the potential value
of insects as feed supplements in poultry production.
The nutritive potential and utilization of termites and earthworms as poultry feed ingredients
have not been documented in Botswana. Therefore, the objective of this work is to create awareness
on the nutritional value of termites and earthworms as sources of protein in poultry diets in
smallholder poultry production.
Termites
Termites (Order: Isoptera) are social insects which build their nests in the soil or wood and
they make up to 95% of the soil insect biomass in lowland tropical rainforests 12. Termites live in
extended colonies and have a significant influence on the surrounding ecosystem. They are social
insects that play the principal detritivorous role in tropical ecosystems. Termites feed on detrital
material and as a result play a major role in decomposition processes, nutrient cycling and carbon
processing 15, 28. Isoptera are especially important in soil formation processes because of their ability
to utilize and recycle cellulose because of the enormity of their biomass and numbers. In addition,
tropical soil dwelling termites exert a profound effect on soil structure affecting many soil properties
including friability, porosity, aeration, organic content, soil permeability and water storage capacity.
In turn, the physical and chemical features of soil environment and its vegetation cover influence the
species composition, diversity, distribution, nesting and foraging habits of termites 11, 13, 51.
Botswana’s termite fauna is ecologically diverse and shows differing preferences of habitats.
This includes economically important species which damage wooden structures. The nest structure
Tiroesele and Moreki, IJAVMS, Vol. 6, Issue 5, 2012: 368-376 DOI: 10.5455/ijavms.174
ALTERNATIVE SOURCES OF PROTEIN FOR POULTRY
can be associated with the species of termites. Nests can be classified as ground mound, subterranean,
pole and tree wood nests 32, 14, 2, 43. According to Banjo et al 7 termites (Macrotermes bellicossus) are
eaten in several parts of western Nigeria. The winged adults are usually caught while on their nuptial
flight or collected from the ground after they have shed their wings and then roasted for consumption.
Nutritional composition of termites
Social insect colonies can be divided into specific physiological units with different colony
members specializing in growth, reproduction, defense, and maintenance. Each of these components
has different nutritional requirements. Thus, colonies should distribute nutrients according to different
individual needs. Different castes of a colony have different metabolic and nutritional requirements;
therefore they require different amounts of micronutrients.
Because of the increasing cost of high quality fish meal required for poultry feed, there is a
need to search for alternative sources of animal protein, especially in developing countries such as
Botswana. Termites are social insects that swarm seasonally, especially at the onset of rainy season or
after a heavy rainfall. The long winged reproductive termite is edible and is highly sort after as a
delicacy. During swarming, a lot of these termites are wasted and could be utilized for production of
fish feeds 44. Previous investigations have suggested the possible use of some alternative animal
protein feedstuffs such as earthworm meal 6, 48 and maggot meal 17, 45.
Table 1. Proximate, mineral content and energy composition (% dry matter) of termites
Composition
Sogbesan and Ugwumba 44
Oyarzun et al 34
Banjo et al 7
Crude protein (%)
46.3
58.20 ± 3.67
21.25
Crude lipid (%)
30.1
15.04 ± 8.6
Crude fibre
7.3%
2.45
Lignin
17.25 ± 3.19%
Cellulose
9.77 ± 1.71%
Ash (%)
3.6
4.11 ± 0.23
2.90
Dry matter (%)
96.4
92.36 ± 4.32
90.05
Sodium
0.20 (g)/100g)
0.17 ± 0.04%
Calcium
0.23(g/100g)
0.26 ± 0.04%
Potassium
0.38 (g/100g)
0.54 ± 0.06%
Phosphorus
0.38 (g/100g)
0.38 ± 0.04%
Magnesium
0.15 (g/100g)
0.14 ± 0.01%
Gross energy
2457.61 (kJ/100g)
6.01 ±0.46 (kcal/g)
Metabolizable
1843.21 (kJ/100g)
Energy
Digestible energy
3040 (kJ/100g)
34
7
44
Source: Oyarzun et al ; Banjo et al ; Sogbesan and Ugwumb
Termites are often included in human diet in many parts of Africa, Latin America, Asia and
Australia 20, 40, 39, 46. The study of Gope and Prasad 20 showed that insects are highly nutritious and
present the cheapest source of animal protein and termites, (Odontotermes feae Linn) are an important
insect food. The nutrient analysis of O. formosanus has revealed a high percentage of protein, lipids
and carbohydrates 52. Termites have notable nutritional value because of their protein, fat (lipid) and
essential amino acid 22, 36, 27. According to Solavan et al 46, termites are among the insects with the
highest fat content. Phelps et al 38 found that the winged sexual forms of the African termites
(Macrotermes falciger) had about 3196 KJ/100 g (dry weight basis) caloric value while M.
Tiroesele and Moreki, IJAVMS, Vol. 6, Issue 5, 2012: 368-376 DOI: 10.5455/ijavms.174
ALTERNATIVE SOURCES OF PROTEIN FOR POULTRY
subhyalinus had about 2575 KJ/100 g (dry weight basis) 33. According to Hickin 23 termites provide
560 calories per 100 g. The findings from the previous investigations show that termites can be used
as a protein source in poultry diets.
Termites are a valuable source of protein, fats and essential amino acids in the diet for both
primates and humans. Termites have crude protein of 81.66% and 87.33% for workers and sexual
forms, respectively 35. These crude protein values suggest that termites can be used a source of protein
in poultry diets to support growth and maintenance of the body of poultry. Proteins maintain acidity
and water balance in the body. Furthermore, Sogbesan and Ugwumb 44 reported crude protein content
of 46.3% in termites. On the other hand, Banjo et al 7 reported crude protein values of 20.4% and
22.1% in Macrotermes bellicosus and M. notalensis, respectively. The carbohydrate content was also
found to be 1.26% for workers and 2.73% for sexual forms. Also, the amino acid content in sexual
and worker forms was 6.77% and 4.66%, respectively. The results of previous studies show that crude
protein content of termites varies widely (20.4 to 87.33%). Table 1 gives proximate analysis, mineral
content and energy levels of termites. It is evident from Table 1 that termites have excellent
nutritional qualities.
Table 2 shows nutrient composition of six feed ingredients. According to Table 2, the crude protein
of termite is higher (70.1%) than that of soybean meal (43.1%) and fish meal (29.7%). In addition,
metabolizable energy (ME) of the termites compares favourably with that of maize (16%) and
soybean (16.3%) but is higher than that of fish meal. However, ash percentage in the termite is lower
(8.3%) compared to fish meal (41.7%). The workers concluded that termites are capable of
completely replacing soybean meal, fish meal and maize meal based diets for growing chicks without
deleteriously affecting growth performance.
Table 2. Nutrient composition of feed ingredients
On Dry matter basis, %
DM, %
CP
EE
NFE
CF
Ash
ME/MJ/kg
Maize meal
85.9
8.2
4.5
82.7
2.2
1.9
16.0
Rice bran
90.0
13.5
12.7
58.5
7.6
7.7
12.6
Soybean
91.0
43.1
15.4
32.6
4.1
4.8
16.3
Fish meal
81.3
29.7
4.4
18.1
6.0
41.7
8.5
Fresh termites
21.0
70.1
7.0
1.2
13.5
8.3
14.1
Fresh larvae
26.5
59.0
23.0
2.62
8.7
6.6
17.5
30
Source: Men et al
DM= dry matter, CP= crude protein, EE= ether extract, NFE= nitrogen free extract, CF= crude
fibre, ME= metabolizable energy, MJ= mega joule
The essential amino acids composition of termite and fish meals are summarised in Table 3. It is clear
from Table 3 that fish meal is superior to termite meal in amino acid concentrations.
According to Banjo et al 7 vitamins A, B2 and C contents in termite meal are 21.25 ug/100 g,
25.35 mg/100 g and 2.40 mg/100 g, respectively. Additionally, calcium, phosphorus, iron and
magnesium in termite meal are 2.45 mg/100 g, 90.05 mg/ 100 g, 2.90 mg/100 g and 43.05 mg/100 g.
The study of Sogbesan and Ugwumba 44 showed that fish meal contains 3530 mg/100 g calcium, 2400
mg/100 g phosphorus, 80 mg/100 g magnesium, 910 mg/100 g sodium and 960 mg/100 g potassium.
These values show that fish meal is superior to termite meal in terms of mineral concentration.
Earthworms
Earthworms (Anellida: Glossoscolecidae) are an important component of the human diet. In
Venezuela, the two species of earthworms that are widely consumed are kuru (Andiorrhinus kuru n.
sp.) and motto (A. motto) 37. Earthworms are a natural food source for poultry kept under free-range
Tiroesele and Moreki, IJAVMS, Vol. 6, Issue 5, 2012: 368-376 DOI: 10.5455/ijavms.174
ALTERNATIVE SOURCES OF PROTEIN FOR POULTRY
systems and, live or dried, are highly palatable to poultry 16. Previous studies have shown that worms
are highly nutritious and have beneficial effects when included in animal diets. Earthworms can be
produced and harvested with ease to feed family poultry.
Table 3. Essential amino acids composition fish meal and termite meal (percent dry matter)
Major animal protein sources
Essential Amino Acids (%)
Fish meal
Termite meal
Inclusion levels of termite meal (%)
Arginine
5.34
3.63
Histidine
4.19
2.65
Isoleucine
2.62
2.32
Leucine
8.31
3.26
Lysine
10.96
6.97
Methionine
2.26
2.08
Phenylalanine
5.52
3.98
Threonine
5.28
3.73
Valine
5.88
3.86
Tryptophan
0.97
0.78
Total EAA
51.33
33.26
Chemical Score
96.7
37.5
EAA/ CP
0.72
0.43
44
Source: Sogbesan and Ugwumba
EAA/CP = Essential amino acids ratio to that of crude protein.
Nutrient composition of earthworms
Various worms are used in poultry diets as a source of protein. Abd Rahman Jabir et al 1 fed super
worm meal to tilapia juveniles (Oreochromis niloticus) and concluded that super worm meal can
replace up to 25% of fish meal protein in fish diet without any adverse effect on feed utilization and
body composition. Reinecke et al 41 in South Africa evaluated protein quality of three species of
earthworms (Eisenia fetida, Eudrilus eugeniae and Perionyx excavatus) and found crude protein
content of E. fetida, E. eugeniae and P. excavatus to be 66.13%, 58.38% and 61.63% compared to
61% for fish meal. This finding shows that the protein content of earthworms differs among species
and also probably due to stage of growth. Furthermore, Paoletti et al 37 found that earthworms contain
large amounts of protein (64.5 to 72.9%), essential amino acids, total fatty acids (6.6 to 10.5 mg/g),
calcium (1020-7070 µg/g) and iron (1050-2990 µg/g) along with notable amounts of other important
elements. The workers concluded that earthworms contain potentially useful quantities of many
nutrients that are critical to the health of humans who eat them. Table 4 presents proximate, mineral
composition (% dry matter) and energy content (kJ/100 g) of earthworm, termite and fish meals.
Ether extract is highly variable among invertebrate species, ranging from 4 to 55% (DMB).
Furthermore, it may vary substantially within species depending on the developmental stage 8.
According to Table 4, earthworm meal has ether extract content of 5.9%. Bernard and Allen 8 stated
that earthworms and night crawlers have less than 20% ether extract (dry matter basis), and contain
ample calcium and appropriate calcium to phosphorus ratios of 1:5:1 to 2.1. The workers argued that
the nutrient composition of annelids is likely to vary depending on the composition of the substrate
(e.g., soil) on which they are grown and/or maintained.
Tiroesele and Moreki, IJAVMS, Vol. 6, Issue 5, 2012: 368-376 DOI: 10.5455/ijavms.174
ALTERNATIVE SOURCES OF PROTEIN FOR POULTRY
The amino acid profile of the three species of earthworms and fish meal is summarised in Table 5. It
is clear from Table 5 that earthworm meals are superior to fish meal in all amino acids except for
serine and tyrosine. It is apparent that E. felida has higher amino acid values compared to other
species of earthworms. Istiqomah et al 26 evaluated the essential amino acid profile of earthworm and
earthworm meal (Lumbricus rubellus) and found that essential amino acid profile of earthworm was
dominated by histidine (0.63% DMB) and that of earthworm meal by isoleucine (1.98% DMB).
Furthermore, the non-essential amino acids of earthworm and earthworm meal were dominated by
glutamic acid (1.52% and 3.60% DMB, respectively). In addition, the value of essential amino acid
index obtained from earthworm meal was higher (58.67%) than those of earthworm (21.23%).
Table 4. Proximate, mineral composition (% dry matter) and energy content (kJ/100 g) of earthworm,
termite and fish meals
Animal Proteins
Nutrient
Earthworm meal
Termite meal
Fish meal
Crude protein (%)
63.0±4.5
46.3±3.2
71.5±4.6
Crude lipid (%)
5.9±1.1
30.1±5.1
8.0±1.4
Crude fibre (%)
1.9±0.2
7.3±1.2
1.2±0.8
Ash (%)
8.9±2.1
3.6±0.6
7.3±1.2
Nitrogen free extract (%)
11.8
19.0
3.2
Moisture (%)
8.6
3.7
8.9
Gross energy (kJ/100 g)
1943.0±1.15
2458.0±60.1
2075.0
Calculated E:P
32.0
53.06
29.03
Metabolizable energy (kJ/100 g)
1476.00
1843.21
1556.05
Digestible energy (kJ/100 g)
16.38
2134.90
1812.70
Sodium (g/100 g)
0.43±0.02
0.20±0.06
0.91±0.006
Calcium (g/100 g)
0.53±0.05
0.23±0.04
3.53±0.15
Potassium (g/100 g)
0.62±0.02
0.38±0.06
0.96±0.006
Phosphorus (g/100 g)
0.94±0.03
0.38±0.08
2.4±0.006
Magnesium (g/100 g)
---------0.15±0.02
0.08±0.002
44
Source: Sogbesan and Ugwumba
Table 5. Amino acid composition of the different protein sources (g/16 g nitrogen)
Amino acid
Eisenia felida
Eudrilus geniae
Perionyx avalus
Fish meal
Threonine
4.47
4.30
4.20
3.84
Serine
4.44
4.5
4.61
14.30
Valine
6.00
5.95
5.88
5.00
Methionine
1.80
1.75
1.90
2.66
Isoleucine
4.60
4.58
4.55
4.06
Leucine
9.80
9.60
9.85
7.80
Tyrosine
3.50
2.95
3.41
3.69
Phenylalanine 3.58
3.20
3.62
3.08
Histidine
3.37
3.10
3.22
2.23
Lysine
7.76
7.85
7.80
7.15
Arginine
9.56
9.20
9.33
4.62
Source: Reinecke et al 41
Tiroesele and Moreki, IJAVMS, Vol. 6, Issue 5, 2012: 368-376 DOI: 10.5455/ijavms.174
ALTERNATIVE SOURCES OF PROTEIN FOR POULTRY
Conclusion: This study has demonstrated the potential utilization of termites and earthworms as
alternative feed resources in terms of protein, mineral and essential amino acid contents for
smallholder poultry production. This information is valuable, especially for the economically weaker
communities in developing countries such as Botswana where poultry feed costs are costly and
beyond reach resource-poor smallholder. More research needs to be done to explore methods of
rearing and processing these insects.
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