Research Article

Amino Acids Composition of Maggot, Earthworm, Termite and Chicken Viscera Meals Used as Proteins Sources in Fish Feeding  

Arnauld S.M. Djissou1 , Isidore Odjo1 , Theophile Godome1 , Shunsuke Koshio2 , Emile D. Fiogbe1
1 Laboratory of Research on Wet Lands, LRZH/FAST/University of Abomey Calavi, Benin
2 Laboratory of Aquatic Animal Nutrition, Kagoshima University, Kagoshima, Japan
Author    Correspondence author
International Journal of Aquaculture, 2018, Vol. 8, No. 23   doi: 10.5376/ija.2018.08.0023
Received: 10 Sep., 2018    Accepted: 17 Oct., 2018    Published: 26 Oct., 2018
© 2018 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Djissou A.S.M., Odjo I., Godome T., Koshio S., and Fiogbe E.D., 2018, Amino acids composition of maggot, earthworm, termite and chicken viscera meals used as proteins sources in fish feeding, International Journal of Aquaculture, 8(23): 168-175 (doi: 10.5376/ija.2018.08.0023)

 

Abstract

The present study was conducted to compare the nutritive value of animal protein sources such as maggot meal (MM), earthworm meal (EM), termite meal (TM) and chicken viscera meal (CM) for fish feeding. Amino acids composition was determined in triplicate by HPLC method. These sources were rich in crude protein (54.30-71.8%), crude fat (10.7-18.7%) and crude fibre (5.7-9.7%). The total amino acid ranged from 18.8 to 57.19 g/100 g of crude protein and the percentages of essential amino acids were 61.58% (MM), 46.21% (EM), 32.02% (TM) and 45.72% (CM). CM was the richest in total acid amino acid (Aspartic acid and Glutamic acid) than other protein sources whereas basic amino acid (Histidine, Lysine and Arginine) was higher in MM than others. Leucine has the most concentrated amino acid in MM, EM and CM whereas there is phenylalanine in TM. Predicted protein efficiency ratio (P-PER1 and P-PER2) values were (2.16, 2.14) MM, (0.68, 0.67) EM, (0.79, 0.27) TM, and (1.20, 1.13) CM respectively; isoelectric point (pI) ranged from 1.10 to 3.65; chemical index (ICh) values were: (1.07) MM, (0.24) EM, (0.11) TM and (0.61) CM. Consequently, the results showed that MM was better at 76.47%, CM in 17.64% while TM was better at 5.88%. Based on these, maggot, earthworm and chicken viscera would be recommended as alternative protein sources to fish meal, especially maggot for fish feeding.

Keywords
Nutritive value; Fish feeding; Predicted protein efficiency ratio

Background

Fishmeal is generally used as the main protein source in those starter feeds, due to its high protein content, balanced amino acid profile, essential fatty acid content, mineral and vitamins content, palatability and high digestibility to most freshwater and marine fish (Médale et al., 2013). Several studies have shown that fish meal improves growth (Young et al., 2002) in fish breeding. However, responses to fish meal tend to be inconsistent because of its variability (Djissou et al., 2016a). Recently, many studies were undertaken to find substitutes with fish meal in order to diversify protein sources for aquafeed and to avoid as well as the production of fish is dependent on a raw material largely majority. Thus, alternative sources to fish meal are tested with various amounts in the fish feeding in order to determine the potentialities of these last.

 

Many scientists have reported the possible use of some alternative animal protein feedstuffs to fish meal such as maggot and earthworm meals (Djissou et al., 2016a), earthworm meal (Sogbesan and Ugwumba, 2006), maggot meal (Sogbesan et al., 2005), poultry dung meal (Fasakin et al., 2000), garden snail meal (Sogbesan et al., 2007), termite meal (Sogbesan and Ugwumba, 2008). Dietary protein is the major and most expensive component of formulated aquafeeds (Wilson, 2002). Of particular interest, the ‘‘least-cost’’ principle of aquafeed formulation has been evolving in recent years towards customer-based aquafeeds, which has led to the concepts of ‘‘functional aquafeeds’’ and ‘‘environmentally oriented aquafeeds’’ (Peng et al., 2008). Invertebrates (maggot, earthworm and termite) and chicken viscera are animal protein sources with low cost, very rich in protein and quite balanced in essential amino acids (Sogbesan et al., 2007). These alternatives must be able to supply adequate essential and non-essential amino acid requirements of the fish or sufficient amino nitrogen to enable their synthesis (Médale et al., 2013) along with dietary energy requirements because its excessive intake may restrict protein consumption and subsequent growth of the fish fed (NRC, 1993).

 

The objective of this study was to compare nutritive value of maggot (Musca domestica), earthworm (Eisenia foetida), termite (Subterranean termite) and chicken viscera meals as alternative protein sources in fish feeding.

 

1 Materials and Methods

1.1 Sample collection and treatment

Following Djissou et al. (2015) method, Vodounnou et al. (2016) method and Sogbesan and Ugwumba (2008) method, samples of maggot (Musca domestica), earthworm (Eisenia foetida) and termite (Subterranean termite) were produced on the research station on the wetlands respectively. Chicken viscera were collected from Agrisatch Society of Ouedo (Benin).

 

1.2 Treatment of samples

After production, maggots, earthworms and termites were collected and cleanly rinsed in water. Maggots were then boiled for 20 min. As for chicken viscera, they were emptied of their droppings. After dejection evacuation, they were washed, drained and cooked on fire. These protein sources were weighed and freeze-dried at 7°C for 24 h in a lyophilisator (EYELA FDU-2110). They were again weighed after the drying operation, and then grinded until to powder form using a milling apparatus.

 

1.3 Chemical analyses

The animal sources were analyzed following AOAC (1990) procedures: crude protein was assessed by the Kjeldahl method after acid digestion using Kjeltec 2300 Auto Analyser (Tecator Höganas, Sweden). The amino acids of feed ingredients were analyzed with HPLC water system (Waters 474, Waters, Milford, MA, USA) including two pumps (Model 515, Waters), an auto-sampler (Model 717, Waters), a fluorescence detector (Model 474, Waters) and a temperature control module. These amino acid analyses were done following the method previously described by Bosch et al. (2006). Thus, aminobutyric acid was added as an internal standard before hydrolyzation. Amino acids were derivatized with AQC (6-aminoquinolyl-N-hydroxysuccinimidyl carbamate) and then separated with a C-18 reverse-phase column Waters Acc. Tag (150 mm 93.9 mm). All these analyses were conducted twice per sample in the Laboratory of Aquatic Animal Nutrition of Kagoshima University (Japan).

 

1.4 Quality parameters determined in animal protein sources

1.4.1 Determination of amino scores (AMSS)

This parameter was first based on the provisional amino acid scoring pattern. In this method, only essential amino acids were scored. Secondly, the amino acid score was calculated using the following formula (FAO/WHO, 1973).

 

 

1.4.2 Determination of the chemical index (Ich)

It is the weakest relationship between the quantity of each essential amino acid contained in protein considered and the quantity of each amino acid corresponding to protein of reference.

 

1.4.3 Determination of the predicted protein efficiency ratio (P-PER)

The P-PER was determined using the equations derived by Alsemeyer et al. (1974), i.e.

 

 

1.4.4 Determination of the isoelectric point (pI)

It was calculated using the equation of the form of Olaofe and Akintayo (2000):

 

 

Where pIm is the isoelectric point of the mixture of amino acids, pIi is the isoelectric point of the ith amino acid in the mixture and Xi is the mass or mole fraction pf the ith amino acid in the mixture.

 

Determination of the total essential amino acid (TEAA) to the total amino acid (TAA), i.e. (TEAA/TAA); total sulphur amino acid (TSAA); total non-essential amino acid (TNEAA), total aromatic amino acid (TArAA), etc.; the Leu/Ile, Lys/Arg, etc. ratios were also calculated.

 

1.5 Statistical analysis

The statistical analysis carried out included the determination of the grand mean, standard deviation (SD) and the coefficients of variation percent (CV%).

 

2 Results

The biochemical composition of maggot meal (MM), earthworm meal (EM), termite meal (TM) and chicken viscera meal (CM) are presented in Table 1. The data indicate that CM meal was rich in crude protein (71.8%) than MM, EM and TM meals (54.6, 56.9 and 54.3%, respectively). The same trend was observed with dry matter and crude fat in CM meal. Essential amino acid composition of fish meal is different from those animal sources of protein (Table 2). Fish meal amino acids values were in 50% higher than those contained in animal proteins sources. Maggot meal was mostly rich in leucine, phenylalanine, histidine, tryptophan and arginine. Table 3 presents the composition of amino acids in the samples (MM, EM, TM and CM). Total amino acids varied from 18.8 g/100 g in TM to 57.19 g/100 g in MM. The quality parameters of amino acids profile in the samples are presented in Table 4. The CV% values varied widely from 0.15-15.98. The TEAA content value ranged from 6.02-35.22 g/100 g of crude protein where MM > CM > EM >TM, whereas TNEAA value varied from 38.42 to 67.98 g/100 g of crude protein. The pI, P-PER and ICh in the samples ranged from 1.10 to 3.65, 0.27 to 2.16 and 0.11 to 1.07, respectively. Minimum and maximum values of these parameters are recorded with termite meal and maggot meal respectively. As for ratios between EAAs, Lys/Arg and Asp/Glu were inferior to 1 in the samples except for Lys/Arg in TM and Asp/Glu in MM. Ratios Lys/Trp and Met/Trp were superior to 1 in the samples except with Met/Trp in MM.

 

Table 1 Biochemical composition (%) of maggot, earthworm, termite and chicken viscera meals

Note: ND-not determined

 

Table 2 Essential amino acids (EAA) content (% dry matter) of fish meal and animal proteins sources

Note: *NRC (2011)

 

Table 3 Amino acid profiles (g/100 g crude protein of dry matter) of maggot meal (MM), earthworm meal (EM), termite meal (TM) and chicken viscera meal (CM)

 

Table 4 Concentrations of essential, non-essential, aromatic, sulphur, etc (g/100 g crude protein) of maggot meal (MM), earthworm meal (EM), termite meal (TM) and chicken viscera meal (CM)

Note: *with His; **without His


Amino acids scores calculated through reference protein showed that all EAA had the lowest score in the termite meal. Isoleucine, phenylalanine, histidine, tryptophan, methionine in earthworm and methionine only in chicken viscera meals had the lowest AMSS (Table 5). Therefore to correct methionine deficiency in the samples, we have added 100/45 or 2.22 times of earthworm meal and 100/62 or 1.61 times of chicken viscera when each of them serves as sole protein source in the diet.

 

Table 5 Essential amino acid scores of maggot meal (MM), earthworm (EM), termite meal (TM) and chicken viscera meal (CM)

 

3 Discussion

The data obtained after analysis, indicate that unconventional source of protein such as maggot, earthworm, termite and chicken viscera meals were rich in crude protein (54.30 to 71.80%) but only chicken viscera meal contained a high level of crude fat (18.7%), whereas low levels of crude fats were obtained for earthworm and termite meals. Analysis results for biochemical composition in MM, EM and TM were different from those reported by several studies (Sogbesan and Ugwumba, 2008; Hasanuzzaman et al., 2010; Adesina, 2012). These differences would be due to the treatment of samples before analysis and the analysis procedures employed. The high crude protein values of these protein sources can be used as alternative protein sources in feeding of fishes. The fish use proteins and lipids which they degrade to cover their energy needs because of their lack capacities to use the food glucids (Médale and Guillaume, 1999) so their ration must thus be rich in proteins and lipids (Médale et al., 2013). Fish meal, a principal ingredient used in the manufacture of fish food, is not essential; it is the nutrient it contains that is important (Médale et al., 2013). Rich in proteins (65 to 72%), fish meal is highly digestible and balanced in amino acids (essential and non-essential), it contains also lipids (5 to 12%) which are not completely eliminated during its manufacture and minerals coming from the skeleton and the scales (Médale et al., 2013). The animal sources of protein such as maggot, earthworm and termite have a lightly low protein rate compared to that of the fish meal except from chicken viscera with comparable rates in crude fats (10.7 to 18.7%). Also, the high digestibility of the animal protein sources (> 90% NRC, 2011), their availability or the possibility of making them available at low cost made of them, a serious potential protein sources in fish feeding.

 

In addition, the sources of proteins must bring the 10 amino acids essential for fish, which are identical for the other animals (NRC, 1993; Médale and Kaushik, 2009). As a whole, the sources of identified proteins contain variable proportions of EAA. Apart from the termite meal, the large majority of the animal protein sources have good EAA contents except for methionine and the tryptophan in the earthworm meal compared to fish meal. Médale and Kaushik (2009) asserted that in the animal protein sources used in fish feeding, the sulphur amino acids (Methionine and Cysteine) are limited. This is justified by the low methionine content in the local sources of proteins compared to that in the fish meal.

 

Generally, the essential amino acids values in those animals sources of proteins don’t satisfy in 20% of cases with EAA requirements of fishes like tilapia and the catfish (NRC, 1993). In TM and EM, all EAA are deficient compared to EAA requirements for tilapia and catfish contrary to the maggots and chicken viscera meals. Leucine and tryptophan in MM and CM meet the requirements of these fishes. These data show that these proteins sources can’t be well utilized only in fish feeding but a mixture of them or with plants protein sources (Watanabe et al., 1998; Collins et al., 2013) can improve growth performances of fishes. This assertion was confirmed by many studies realised on Clarias gariepinus (Djissou et al., 2016a), Heterobranchus longifilis (Sogbesan and Ugwemba, 2008) and Oreochromis niloticus (Djissou et al., 2016b). Leucine is the highest concentrated EAA in MM, EM and CM (6.35 g/100 g, 3.12 g/100 g and 4.20 g/100 g, respectively). Similar observations were also reported by Djissou et al. (2016c) in Dialum guineense, Adeyeye (2011) in raw wheat and millet samples.

 

With regard to quality parameters of protein in the samples, the EAA range between 6.06 g/100 g CP to 35.22 g/100 g CP. These values were far from the values 56.6 g/100 g CP of the egg reference protein (Paul et al., 1976) but slightly close to 23.38 g/100 g CP for Azolla filiculoides meal; 23.2 g/100 g CP for Moringa oleifera meal and 37.96 g/100 g CP for Dialum guineense (Djissou et al., 2016c). But the value of EAA in TM was also far for the value of EAA in termite reported by Sogbesan and Ugwumba (2008). The percentages of EAA for all the samples except TM (61.58 (MM), 46.21 (EM) and 45.72 (CM)) could be favorably compared with that of beach pea protein isolated (43.8-44.4%) (Chavan et al., 2001), Azolla filiculoides, Moringa oleifera and Dialum guineense (42.16-45.73) (Djissou et al., 2016c). The experimentally determined PER usually range from 0.0 for a very poor protein to a maximum possible of just over 4 (Adesina, 2012). The P-PER calculated in the samples meaning that the physiological utility in the body of maggots would be much better than others proteins sources. On the average, these sources would be much better than the sorghum (with P-PER of 0.0-0.29) (Adeyeye, 2008) but only maggot than in millet (P-PER: 1.32-1.66) (Adeyeye, 2009). The values of P-PER showed that these animals’ protein sources are good quality (except EM and TM with low P-PER) and closed by P-PER values of some fishes such as Clarias anguillaris (2.22) and Oreochromis niloticus (1.92) (Salunkhe and Kadam, 1998). Leu/Ile balance is more important than dietary Leu excess alone in regulating the metabolism of Trp and hence the disease process (Gopalan, 1971; Adesina, 2012). The current report shows Leu/Ile to range from 2.08 to 3.36 in samples with a low Leu/Ile in maggot meal. These results were in agreement with studies of Adesina (2012) in maggot, earthworm and soybean and Djissou et al. (2016c) with Azolla filiculoides, Moringa oleifera and Dialum guineense.

 

The isoelectric point (pI) is the minimum pH at which the protein becomes soluble, thus, in preparing the isolate of protein of any given sample, the pI becomes highly important. From the present report, the pI ranged 1.10-3.65, showing that the minimum solubility pH would be just above 1.0. The ratios of Lys/Trp and Met/Trp in the current report were: 1.33-22.33 and 0.57-6.33, respectively. The values were however much better than the values reported for raw, roasted and cooked dehulled Treculia Africana (Adesina and Adeyeye, 2016). The chemical index (ICh) ranged from 0.11 to 1.07. ICh is useful as a rapid tool to evaluate food formulations for protein quality, although it does not account for differences in protein quality due to various processing methods or certain chemical reactions (Nielsen, 2002). These values are higher than those reported by Djissou et al. (2016c) and show that animal protein sources are of good quality than plant protein sources. Also, the amino acid score shows that MM and CM would have been used as only protein source in the diet but EM and TM must be completed by other protein sources (animal or vegetable) in diets of fishes. When the food contribution in amino acids is not precisely adapted to the needs for the animal, nitrogenized catabolism increases, the proteinic retention is reduced and they increased nitrogenized rejections (Médale and Kaushik, 2009). To avoid the deficiencies, the animal sources are mixed and if necessary, of the amino acids of synthesis are added in crystalline form (Djissou et al., 2016a).

 

4 Conclusion

The present study indicates that maggot, earthworm, termite and chicken viscera were rich in crude protein. In term of protein quality, maggot appears the first, then chicken viscera and earthworm and finally the termite. These animal sources of protein can be used as raw materials in feed formulations for replacement of fish meal.

 

Authors’ contributions

All authors, ASMD, IO, TG, SK and EDF have made adequate effort on all parts of the work necessary for the development of this manuscript according to his expertise. All authors read and approved the final manuscript.

 

Acknowledgements

Financial support was provided by Japan International Cooperation Agency (JICA) through Laboratory of Aquatic Animal Nutrition, Kagoshima University, Japan.

 

References

Adesina A.J., 2012, Comparability of the proximate and amino acids composition of maggot meal, Earthworm meal and soybean meal for use as feedstuffs and feed formulations, Elixir Applied Biology, 51: 10693-10699

http://www.elixirpublishers.com/articles/1351342003_51%20(2012)%2010693-10699.pdf

 

Adesina A.J., and Adeyeye E.I., 2016, Comparability of the amino acids composition of raw, roasted and cooked dehulled Treculia africana seeds flour consumed in Nigeria, EC Nutrition, 3: 700-713

https://www.ecronicon.com/ecnu/pdf/ECNU-03-000098.pdf

 

Adeyeye E.I., 2008, The inter-correlation of the amino acid quality between raw, steeped, and germinated guinea corn (Sorghum bicolour) grains, Bulletin of chemical society of Ethiopia, 22(1): 11-17

https://doi.org/10.4314/bcse.v22i1.61320

 

Adeyeye E.I., 2009, The inter-correlation of the amino acid quality between raw, steeped, and germinated pearl millet (Pennisetum typhoides) grains, Pakistan Journal of Science and Industrial Res., 52(3): 122-129

http://www.pjsir.org/documents/journals/22102009005019_PJSIR_52(3)09-Enc.pdf#page=8

 

Adeyeye E.I., 2011, Relationship in amino acid quality between raw, steeped and germinated wheat (triticum durum) grains, Bangladesh J Sc. Ind. Res., 46(1): 89-100

https://www.banglajol.info/index.php/BJSIR/article/view/8112

 

Alsemeyer R.H., Cunningham A.E., and Happich M.L., 1974, Equations to predict PER from amino acid analysis, Food Technology, 28: 34-38

 

AOAC, 1990, Official methods of analysis 15th ed. association of official analytical chemists, Arlington, VA, USA, pp.1298

 

Bosch L., Alegria A., and Farré R., 2006, Application of the 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate (AQC), reagent to the RP-HPLC determination of amino acids in infant foods, J. Chromatogr. B Anal. Technol. Biomed. Life Sci., 831: 176-178

https://doi.org/10.1016/j.jchromb.2005.12.002

 

Chavan U.D., Mckenzie D.B., and Shaludi F., 2001, Functional  properties  of  protein  isolates  from  beach  pea (Lathynes maritimus L.), Food Chemistry, 74: 177-187

https://doi.org/10.1016/S0308-8146(01)00123-6

 

Collins S.A., Overland M., Skrede A., and Drew M.D., 2013, Effect of plant protein sources on growth rate in salmonids: meta-analysis of dietary inclusion of soybean, pea and canola/rapeseed meals and protein concentrates, Aquaculture, 400: 85-100

https://doi.org/10.1016/j.aquaculture.2013.03.006

 

Djissou A.S.M., Tossavi E.C., Vodounnou J.D., Toguyeni A., and Fiogbé E.D., 2015, Valorization of agro-alimentary waste for a production of maggots like source of proteins in the animal feeds, Int. J. Agri. & Agri. R., 7(6): 42-46

http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.736.8405&rep=rep1&type=pdf

 

Djissou A.S.M., Adjahouinou C.D., Koshio S., and Fiogbe E.D., 2016a, Complete replacement of fish meal by other animal protein sources on growth performance of Clarias gariepinus fingerlings, Int. Aquat. Res., 8(4): 333-341

https://doi.org/10.1007/s40071-016-0146-x

 

Djissou A.S.M., Tossavi C.E., Toguyeni A., and Fiogbe E.D., 2016b, Complete replacement of fish meal by unconventional proteins sources in diet of Oreochromis niloticus (L., 1758) fingerlings: growth performance, feed utilization and body composition, IJFAS, 4(5): 242-247

 

Djissou A.S.M., Tossavi C.E., Kpogue D.S., Toguyeni A., and Fiogbe E.D., 2016c, Comparability of amino acids composition in leaves of Azolla filiculoides, Moringa oleifera and Dialum guineensis as sources of proteins in food of fish, IJIAS, 17(2): 718-725

 

FAO/WHO, 1973, Energy and protein requirements, Technical Report Series No.522, World Health Organization, Geneva, 1973

 

Fasakin E.A., Falayi B.A., and Eyo A.A., 2000, Inclusion of poultry manure in the diet for Nile Tilapia (Oreochromis niloticus, Linneaus), Journal of Fish.Tech., 2: 51-56

 

Hasanuzzaman A.F.Md., Hossian Sk.Z., and Das M., 2010, Nutritional potentiality of earthworm (Perionyx excavates) for substituting fishmeal used in local feed company in Bangladesh, Mesopot. J. Mar. Sci., 25(2): 134-139

https://www.iasj.net/iasj?func=fulltext&aId=33985

 

Médale F., and Kaushik S., 2009, Les sources protéiques dans les aliments pour les poissons 406 d’élevage, Cahiers d’Agriculture, 8(2-3): 103-111

http://revues.cirad.fr/index.php/cahiers-agricultures/article/download/30777/30537

 

Médale F., Le Boucher R., Dupont-Nivet M., Quillet E., Aubin J., and Anserat J., 2013, Des aliments à base de végétaux pour les poissons d’élevage, INRA Production Animale, 26(4): 303-316

http://archimer.ifremer.fr/doc/00200/31166/29565.pdf

 

Médale F., and Guillaume J.C., 1999, Nutrition énergétique, In: Nutrition des poissons et des crustacés, Guillaume J., Kaushik S., Bergot P., Métailler R. (Eds), INRA, Paris, France, pp.87-111

 

Nielsen R., 2002, Mapping mutations on phylogenesis, Systematic Biology, 51(5): 729-739

https://doi.org/10.1080/10635150290102393

 

NRC, 1993, National Academy Press Washington, D.C., USA, pp.105

 

NRC, 2011, National Academy Press Washington, D.C., USA, pp.405

 

Olaofe O., and Akintayo E.T., 2000, Prediction of isoelectric points of legume and oilseed proteins from their amino acid compounds, J.Technol Sci., 4: 49-53

 

Paul A.A., Southgate D.A., and Russel J., 1976, First Supplement to McCance and Widdowsons, The composition of foods, HMSO, London

 

Peng L., Kangsen M., Jesse T., and Guoyao W., 2008, New developments in fish amino acid nutrition: towards functional and environmentally oriented aquafeeds, Amino acids

https://doi.org/10.1007/s00726-008-0171-1

 

Salunkhe D.K., and Kadam S.S., 1998, Handbock of world food legumes: nutritional, chemistry, processing, technology and utilization, CRC Press, Boca Raton, FL

 

Sogbesan A.O., and Ugwumba A.A.A., 2008, Nutritional evaluation of termite (Macrotermes subhyalinus) meal as animal protein supplements in the diets of Heterobranchus longifilis (Valenciennes, 1840) Fingerlings, Turk. J. Fish. Aquat. Sci., 8: 149-157

http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.607.6185&rep=rep1&type=pdf

 

Sogbesan O.A., Ugwumba A.A.A., Madu C.T., Eze S.S., and Isa J., 2007, Culture and utilization of earthworm as animal protein supplement in the diet of Heterobranchus longifilis Fingerlings, Turk. J. Fish. Aquat. Sci., 2: 375-386

https://doi.org/10.3923/jfas.2007.375.386

 

Sogbesan O.A., and Ugwumba A.A.A., 2006. Bionomics evaluation of garden snail (Limicolaria aurora, Jay, 1937; Gastropoda: Limicolaria) meat meal in the diet of Clarias gariepinus fingerlings (Burchell, 1822), Nigerian Journal of Fisheries, 2(3): 358-371

 

Sogbesan O.A., Ajuonu N.D., Ugwumba A.A.A., and Madu C.T., 2005, Cost benefits of maggot meal as supplemented feed in the diets of Heterobranchus longifilis × Clarias gariepinus (Pisces-Clariidae) hybrid fingerlings in outdoor concrete tanks, Journal of Industrial and Scientific Research, 3(2): 51-55

 

Vodounnou D.S.J.V., Kpogue D.N.S., Tossavi C.E., Mensah G.A., and Fiogbe E.D., 2016, Effect of animal waste and vegetable compost on production and growth of earthworm (Eisenia foetida) during vermiculture, Int. J. Recycl. Org. Waste Agricult, 5(1), 87-92

https://doi.org/10.1007/s40093-016-0119-5

 

Watanabe T., Verakunpiriya V., Watanabe K., Viswanath K., and Satoh S., 1998, Feeding of rainbow trout with non-fish meal diets, Fish Sci., 63: 258-266

https://doi.org/10.2331/fishsci.63.258

 

Wilson R.P., 2002, Protein and amino acids, In: Halver JE, Hardy RW (eds) Fish Nutrition, 3rd version, Elsevier Science, San Diego, USA, pp.144-179

 

Young M.G., Tokach M.D., Goodband R.D., Nelssen J.L., Dritz S.S., and Cici M., 2002, Comparison of international protein corporation 740 fish meal and special select menhaden fish meal in nursery pig diets, J. Anim. Sci., 80(Suppl. 2): 59 (Abstr.)

http://newprairiepress.org/cgi/viewcontent.cgi?article=6700&context=kaesrr

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