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ANIMAL HUSBANDRY & VETERINARY SCIENCE | RESEARCH ARTICLE

Potential of earthworm (Eisenia foetida) as
dietary protein source for rohu (Labeo rohita)
advanced fry
Kedar Nath Mohanta, Sankaran Subramanian and Veeratayya Sidweerayya Korikanthimath

Cogent Food & Agriculture (2016), 2: 1138594

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04 g) Goa. Environment & Agriculture.2*. 23. Therefore. respectively) and earthworm custard (0.0 license.84. At the end of experiment. 3. Mohanta et al. protein efficiency ratio. The formulat- Research Complex for Goa. 14. Kausalyaganga. Additional information is available at the end of the article 2. and energy retention efficiency (%) of fish fed pel- Pedro González-Redondo. Sankaran Subramanian1 and Veeratayya Sidweerayya Korikanthimath1 Received: 22 August 2015 Abstract: Earthworm. rohu.21. a non-conventional protein source with 520–530 g protein kg−1 Accepted: 27 December 2015 on dry matter basis was used in three forms viz. Fish and Fishery Science.21.71 ± 0.58.53. Dr. 1. Fish Nutrition and Physiology Division. India continuous aeration were used for rearing the fish. India. involved in study on nutrient requirement and could be used as potential fish feed ingredient for cost-effective diet development of carp and nursery rearing of fish. India.1138594 ANIMAL HUSBANDRY & VETERINARY SCIENCE | RESEARCH ARTICLE Potential of earthworm (Eisenia foetida) as dietary protein source for rohu (Labeo rohita) advanced fry Kedar Nath Mohanta1. In the present study we have evaluated the projects.12.42. University of Seville. Food Science & Technology Keywords: earthworm. management process or organic farming is very Bhubaneswar. 4. Dr. The 300 Institute of Freshwater Aquaculture..93. 0. protein. 10. The present work is an nutritionally balanced low-cost feed for rohu fry.34. The of fish and the other on improvement in protein study results would be helpful in formulating use efficiency of carp diet.1080/23311932. Goa. he is working as Principal the suitable non-conventional alternate protein Scientist in Fish Nutrition and Physiology Division sources. The first author. Bhubaneswar 751002. Mohanta is mainly rich in protein and polyunsaturated fatty acid.94. the by-product of waste of Central Institute of Freshwater Aquaculture.0 MJ kg−1 diet) experimental diets. very limited research Kedar Nath Mohanta freshwater ornamental fish for nursery and has been carried out on use the earthworm in fish grow-out stages.19. ICAR protein kg−1 diet) and iso-caloric (17. This open access article is distributed under a Creative Commons Attribution (CC-BY) 4. and 18. 0.18. a waste product of vermicompost in formulating the low-cost diet for carps. non-conventional feeding. Page 2 of 13 . attempt to utilize earthworm. and (iii) pelleted earthworm diet to prepare three iso-nitrogenous (500 g *Corresponding author: Kedar Nath Mohanta.05) than the corresponding values of whole earthworm (1. respectively) fed diets.62. L fiberglass-reinforced plastic tanks containing 100 L of water with the provision of Downloaded by [157. diet.26. and 11. India is involved in sources particularly the fish meal and oilcakes both strategic and applied research to develop used in fish feed due to their extensive use and nutritionally balanced cost-effective diet for stiff competition from other animal production food and ornamental fish. The experiment results indicated that the pelleted earthworm diet could be used in rearing of rohu advanced fry. 2.doi.50.0.2016.38. Ela. Spain leted earthworm diet (2. and 8. Currently he has two research diet.10] at 07:06 19 September 2017 Odisha.org/10. an Kedar Nath Mohanta was a Senior Scientist in intensive research efforts have been made by fish ICAR RCG. Subjects: Bioscience. 10 fish were stocked. (i) whole earthworm (ii) earthworm First Published: 19 January 2016 custard. sectors like dairy and poultry. Labeo rohita ABOUT THE AUTHORS PUBLIC INTEREST STATEMENT The research group of ICAR Research Complex There is an acute shortage of conventional protein for Goa (ICAR RCG). Cogent Food & Agriculture (2016). Old ed diets were fed ad libitum twice daily to Labeo rohita advanced fry (0. © 2016 The Author(s). 3. 1. the E-mail: knmohanta@gmail. Goa 403402. 2: 1138594 http://dx.30. respectively) was sig- nificantly better (p < 0. Goa where the present work was nutritionists around the globe to identify and use carried out. Central in triplicates for a period of 35 days. So far. food conversion ratio.com weight gain (g).6. Reviewing editor: protein retention efficiency (%). one on development of appropriate earthworm (Eisenia foetida) as alternate dietary feeding strategies based on compensatory growth protein source in Labeo rohita advanced fry. In each replicate. Earthworm. specific growth rate. Presently.48.

Vidna. Guerrero. 2008. Experimental diets Except earthworm. Detritivorous terres- trial and aquatic Oligocheate worms are well known for their capacity to break down and utilize human and animal wastes (Guerrero. ω-3 fatty acids). Nandeesha. Pereira & Gomes. 1983. earthworm (Eisenia foetida) has been proven the most promising and successful till date for vermiculture (Hartenstein. 1981). Introduction Vermiculture.12. 1988. The earthworm was kept unfed for 48 h so as to eliminate all the feed contents that remained earlier in the gut. Pereira & Gomes.. 1994). Pujic. 1988. 1988.1975. Several researchers have reported the use of earthworm as dietary protein source either alone or in combination with other feed ingredients in formulating the fish diets (Edwards & Niederer. 1987.10] at 07:06 19 September 2017 fraction of earthworms conducted by Hansen and Czchanska (1975) revealed a high proportion of polyunsaturated fatty acids (linolenic. 2008. and earthworm were oven-dried for 24 h at 105°C and then finely powdered using a mixer grinder and sieved through a fine-meshed screen (0. & Seenappa. 2: 1138594 http://dx.. Tacon. Goa. mainly the lesser sardines of family Engrolidae and ribbon fish of family Trichuridae available in the locality. 1985.5 mm diameter). 2006. & Kaplan. India). and hen’s egg (Premium meat supplier. the details of which are presented in Table 1. Reinecke & Alberts. gelatin (Himedia. 1993). 2003. Mumbai. Srikanth. Guerrero. 1976). it can be used as a potential non-conventional animal protein source for formulating the fish feed (Pereira & Gomes. 1979.1080/23311932. & Das. 1982. India). a century old practice is now being revived worldwide for waste management. Reinecke & Alberts. 2003. sus- tainable organic agriculture. Das. all the other required fish feed ingredients viz.doi. Tacon.. Devaraj. India). Among the various terrestrial worms. But. The protein and lipid contents of earthworm is varying from 50 to 70% and 5 to 10%. 1990). Istiqomah. Stafford. neither solvent extracted nor dehulled). Sogbesan and Ugwumba (2008a) reported that the quantity of sodium. 1994). Sogbesan & Madu. & Oyarzun. Stafford. vegetable oil (Marico Industries Limited. & Toress. Guerrero. 2. Cova. Tacon. Damayanti. mineral and vitamins (EMIX PLUS..48. & Julendra. 2002. and potassium available in the earthworm is sufficient in meeting the requirement levels for cat fish and all tropical fish (NRC. Carlos. Hartenstein et al. Velasquez. mechanical extraction of oil). & Edwards.1. groundnut oil cake. 1994) and it contains variable lipid contents naturally high in ω-3 fatty acids (Dynes.2016. so far the available literature on use of earthworm in formulat- ing the carp diet is very limited. 1981. 1983. and aquaculture (Chakrabarty. Medina et al. Anand. 1995. Sofyan. 1991. 2003. Keshavappa. Tacon. India). 1979. Although the earthworm is considered as a by-product of waste management process or vermi- culture unit. Tacon.org/10. Watanabe & Tsukamoto. which is essential for formulating fish feed of many species. Hilton. Medina. 1989. Mumbai. Ibañez. lean prawn (Acetes indicus) meal. 1987.1138594 1. Earthworm effectively converts the waste materials to loose friable compost with potential value as a plant growth medi- um. 1983. Neuhauser. Lieberman. as reported by several earlier researchers (Dynes. Panaji. 2009. 1976). foetida) was procured from a local vermicompost unit (Margao. Labeo rohita advanced fry. Watanabe & Tsukamoto. 1983. 2009). Considering the high nutrient value of earthworm and its huge pro- duction potential in the coming years as by-product of vermiculture and waste management processes. respectively. et al. calcium. The proximate composition of the ingredients was determined (Association of Official Analytical Chemists. 1984. & Edwards. groundnut oil cake (de- oiled groundnut. Cogent Food & Agriculture (2016). Basavaraja. Mohanta et al. Reinecke & Alberts. Three experimental diets were prepared in which the earthworm was used in three forms as de- scribed below: Page 3 of 13 . 1995. The fish meal. Earthworm has been found to be a good source of protein with favorable amino acids (Guerrero. 1995). lean prawn. Materials and methods 2. skimmed milk powder (Amul India. Sogbesan & Madu. Stafford & Tacon. Gujarat. Kostecka and Paczka. Hansen & Czochanska. The earthworm (E. Extensive analysis of the lipid Downloaded by [157. Herrera. India) were procured from the local market. Mumbai. 2003. India). 1987. 1981. fish meal (sun-dried miscellane- ous marine trash fish. a study was undertaken to evaluate the possibility for use of different forms of earth- worm in formulating the diets of rohu.

and a dough of feed mix was prepared.0 Prawn meal 926 481 45.12. respectively. After the gelatin is dissolved properly. 2: 1138594 http://dx. Then the mineral and vitamin mix was added and the whole feed mix was evenly mixed using the kitchen mixer grinder. mineral and vitamin mix and vegetable oil were mixed thoroughly using a kitchen mixer (Philips India Limited. The dough was put in to an alu- minum container and steam cooked for 20 min using a domestic pressure cooker (Hawkins Make. blended properly. Mumbai) and the earthworm meal was prepared. Page 4 of 13 . Whole earthworm diet (D-1) Downloaded by [157. fish meal. and then ground using a kitchen mixer grinder (Philips India Limited. For daily feeding of the earthworm custard. Mumbai).5 mm size) using a sharp knife and stored in a refrigerator at 4°C until use. All the experimental diets used were iso-nitrogenous (500  g protein kg−1 diet) and iso-caloric (17. After the gelatin is dissolved properly..0 153.3.org/10. Pelleted earthworm diet (D-3) For preparation of pelleted earthworm diet.0 76. Mumbai). ground- nut oil cake. The required quantity of lukewarm water was added to the feed mix. A desired quantity of water was heated in a 1 L beaker to 80°C by using an electric heater and the required amount of gelatin was dissolved into it with slow stirring. first the earthworm was boiled for 45 min in water adding a pinch of common salt. A desired quantity of water was heated in a 1-L beaker to 80°C by using an electric heater and the required amount of gelatin was dissolved in to it with slow stirring.2016.1.2. thoroughly washed with clean water and chopped into pieces (0. it was added to the feed mix.0 69. Mumbai. prawn meal.1138594 Table 1. The dough was passed through a hand pelletizer to obtain 2 mm diameter feed pellets. a piece of earthworm custard was taken and cut in to small pieces (0. and a dough of feed mix was pre- pared. India) to obtain the earthworm custard. it was added to the feed mix. Then it was oven-dried for 24 h and powdered with a kitchen grinder (Philips India Limited.2 Groundnut oil cake 935 445 75.1. 2.3 Hen’s egg 260 480 456 12 35 Skimmed milk powder 920 370 15 8 3 Gelatin 950 910 5 7 68 2. The ingredient and chemical composition of the experimental diets are presented in Tables 2 and 3.1. Earthworm custard (D-2) For preparation of earthworm custard. The earthworm custard was cooled at room tem- perature and stored in a refrigerator at 4°C until use. The required quantities of dried earthworm meal. washed thoroughly in clean water.5 Fish meal 922 562.5 mm) with a kitchen knife and fed to the experimental fish.0 86.1080/23311932. Cogent Food & Agriculture (2016). The required quantities of skimmed milk powder and hen’s egg (yolk + albumin) were added to the ground earthworm and mixed thoroughly.1.6 18. Proximate composition (g kg−1 dry matter basis) of feed ingredients used for formulating the experimental diets Ingredients Dry matter Crude protein Ether extract Crude fiber Total ash Earthworms 170 520 180 78 126. The pellets were dried at 60°C and stored in a refrigerator at 4°C until use.doi.0 182.0 MJ kg−1 diet).48.5 81. 2. The required quantity of lukewarm water was added to the feed mix.10] at 07:06 19 September 2017 The whole earthworm (after 48 h of fasting) were boiled (with a pinch of common salt) in water. Mohanta et al. blended properly. at first the earthworm was boiled in water for 45 min adding a pinch of common salt and washed thoroughly in clear water as described above.

L-lysine: 4 g.000 IU. the fish were fed with a fish meal-oil cake-rice bran-based prepared diet (crude protein: 400 g protein kg−1 diet. The unconsumed feed and excreta were removed everyday by siphon- ing at 0730 and 1530 h and the unconsumed feed with respect to each tank was oven-dried over- night at 105°C and stored separately in the refrigerator at 4°C. Calcium Pantothenate: 1. average weight ± SE) were stocked randomly in triplicate tanks for each dietary treat- ment following a complete randomized design.97 17. The tank wise pooled unconsumed feed sample collected over a period of 35 days was used for calculating the total feed consumption and feed conversion ratio (FCR) after the experiment was completed.40.71 ± 0. Choline Chloride: 60 g. In addition to this. Ca: 200 g. Page 5 of 13 . Co: 180 mg.10] at 07:06 19 September 2017 D3: 4.04 g. Mumbai. Mohanta et al.. Vitamin B6: 400 mg. India) with a generator back up (Kirloskar. energy: 16.000 IU. Selenium: 20 ppm.000 mg.2.48. India). about 50% of the water was exchanged in every three days interval. ether extract: 120 g kg−1 diet.000 mg.800 mg. DL-Methionine: 4 g. Fe: 3.000 mg. Government of Goa (India) and acclimatized to the laboratory condition for 15 days using two 1000 L fiber-reinforced plastic (FRP) tanks under the provision of continuous aeration using an electrically operated air-blower (Roots Air Blower. Cu: 800 mg.56 17.4 mg. Mn: 10. Proximate composition (g kg−1 dry matter basis) of the experimental diets Parameters D-1 (Whole D-2 (Earthworm D-3 (Pelleted earthworm diet) custard diet) earthworm diet) Dry matter 182 450 923 Crude protein 520 508 501 Ether extract 160 150 180 Crude fiber 35 18 85 Ash 124 79 126 Gross energy (MJ kg−1) 17. groups of 10 healthy and uniformly sized advanced rohu fry (0. During acclimatization. Vitamin B12: 2. Nicotinamide: 4 g. Zn: 2.org/10. Vitamin Downloaded by [157.1138594 Table 2.72 MJ kg−1 diet). The water lost during the re- moval of unconsumed feed and excreta by siphoning was replenished with the seasoned freshwater every day. Mumbai.1080/23311932. Table 3. Ingredient composition (g kg−1) of the experimental diets Ingredient D-1 (Whole D-2 (Earthworm D-3 (Pelleted earthworm diet) custard diet) earthworm diet) Earthworm 1000 600 400 Fish meal – – 100 Groundnut oil cake – – 300 Prawn meal – – 100 Skimmed milk powder – 100 – Hen’s egg – 220 – Gelatin – 60 60 Vitamin & mineral – 20 20 mixture* Vegetable oil – – 20 *Composition of Vitamin and Mineral mix (EMIX PLUS. P: 120 g. India) (Quantity/kg): Vitamin A: 22. 2: 1138594 http://dx. Experimental design and fish maintenance Four hundred rohu advanced fry (average weight 0. Cogent Food & Agriculture (2016). Kolkata. Vitamin E: 300 mg. The experimental fish were fed ad libitum twice daily (0830 and 1630 h) to their respective diets for a period of 35 days.12. I: 400 mg. Vitamin B2: 800 mg.14 2. Vitamin K: 400 mg.doi.48 g) were procured from the Anjunem hatchery of the State Fisheries Department.2016. After 15  days of acclimatization.00. Three hundred liter FRP tanks containing 100-L water (static water system) were used for rearing the fish.

doi.25%).7. dissolved oxygen. Statistical analysis The difference among the treatments was tested by one-way analysis of variance (ANOVA) and comparison between the treatments was done by Duncan’s multiple range test at p  <  0.05. 1986). the other water qual- ity parameters such as temperature. Ether extract was de- termined by solvent extraction with petroleum ether. The water quality parameters in experimental tanks were in the range of Temperature (°C): 25. Gross energy in diets and fish body was calculated by using Bomb Calorimeter (Parr.06–0. Dry matter was estimated by oven-drying the samples at 105°C till a constant weight and crude protein percent was calculated by estimating ni- trogen content by micro-Kjeldahl method and multiplying with a factor 6. total hardness. Nitrate Nitrogen (mg L−1): 13.4. Ammonia Nitrogen (mg L−1): 0.04–0. the feed and nutrient consumption with respect to each dietary treatment were calculated on dry mat- ter basis as the dry matter contents of three experimental diets used were varied widely among them.25%) followed by alkali digestion (1.8–7. The final weight was recorded at the end of the experimental period by batch weighing of the fish. pH: 7. ammonia ni- trogen (NH3-N). 1990). 2. 2.3. IL.48. 2. Downloaded by [157.1080/23311932.25. Cogent Food & Agriculture (2016). Parr Instrument Company. Similarly.org/10.6. the total feed consumed in wet weight was converted to dry weight (total feed consumed in wet weight × % of dry matter content of the respective diets) and it was divided by weight gain of fish (wet weight). for 10–12 h.6–26.2–116. and nitrite nitrogen (NO2-N) of the experimental tanks were analyzed every week (American Public Health Association. and ERE).5.2–7. The Page 6 of 13 .10] at 07:06 19 September 2017 2.% = × 100 Protein/Energy intake For calculating the FCR of the fish fed whole earthworm diet (D-1) and the earthworm custard diet (D-2).5.5.09.1138594 The experimental tanks were supplied with continuous aeration throughout the experiment period by using an electrically operated air-blower as mentioned above. The seasoned and aerated ground- water was used for rearing the fish. for calculating the other nutritional parameters (PER. boiling point 40–60°C. The natural light cycle was 12  h light/12  h darkness for the experiment. 1989). Calculation of nutritional indices The different nutritional indices were determined as follows: ( ) ln final weight − ln initial weight Specific growth rate SGR = ( ) × 100 Experimental duration days ( ) ) Total feed intake dry weight ( Feed conversion ratio FCR = × 100 Total live weight gain Total live weight gain Protein efficiency ratio (PER) = Total protein intake ( ) Protein/Energy gain in body Protein/Energy retention efficiency PRE/ERE. Nitrite Nitrogen (mg L−1): 0. 2: 1138594 http://dx. model 1341. PRE. Chemical analyses The proximate composition of experimental diets and whole body was analyzed in triplicates (Association of Official Analytical Chemists. USA). Dissolved Oxygen (mg L−1): 6.2016. Moline.0–18. Mohanta et al.3 which were found to be in the normal range of carp rearing (Renukaradhya & Varghese. total alkalinity.12.08. Total ash content was determined by incinerating the sample at 650°C for 6 h and crude fiber by acid digestion (1.. Water analyses Except water temperature which was recorded twice daily (0830 and 1430 h).0 and Total Alkalinity (mg CaCO3 L−1): 95. nitrate nitrogen (NO3-N).

05b 3. Values are the means of three samples ± standard error (SE) for each experimental diet.04a Feed conversion ratio (FCR) 2. 2: 1138594 http://dx.38 ± 0.38 ± 0.3d Gross energy (kcal/g) 5.0 ± 0.08a % day−1) Protein efficiency ratio 0.05) in moisture and energy contents among the three dietary treatment groups.2a 743 ± 6.84  ± 0.35 ± 0.12b 8. the growth and dietary indices as mentioned above of the former group was better than the later group.53 ± 0.03a 5.5 a 98. The whole body composition of fish (Table 5) indicated that there was no variation (p > 0.1138594 Table 4.56 ± 0. and protein and energy retention and lowest food con- version ratio (p < 0. The total ash content was significantly lower (p < 0.6 ± 0.6a Crude protein 652.16c 23. Cogent Food & Agriculture (2016).26 ± 0. the whole body ether extract content of fish fed pelleted earthworm diet was significantly lower (p < 0. rohita (g kg−1 dry matter basis) advanced fry before and after the experiment Parameters Initial Final D-1 (Whole D-2 (Earthworm D-3 (Pelleted earthworm diet) custard diet) earthworm diet) Moisture 756 ± 5.05).04a (PER) Protein retention efficiency 14. But the whole body pro- tein content of fish was significantly higher (p < 0.03a 5.08b 1.4c 100.5 a 140.03a Final weight (g) 2. specific growth rate.03a 1.0c 668.42 ± 0.02a Note: Mean values with the same superscripts in each row are not significantly different (p > 0.62 ± 0.8 ± 0.8±0.01c 1.06c 4.5c 662.6 ± 0.5 a 135.6 ± 0.12..04a 5.50 ± 0.66 ± 0. 3.68a (PRE) Energy retention efficiency 11.03c 2.05c Specific growth rate (SGR.40 ± 0.01b 0. release v6.05) in fish fed pelleted earthworm diet followed by whole earthworm and earthworm custard diets.48.0a 736 ± 4.10] at 07:06 19 September 2017 (ERE) Note: Mean values with the same superscripts in each row are not significantly different (p > 0.05) than the other two diet fed groups.6 a 139.03a 0.2 ± 0. However.org/10.5 b 92.05).71 ± 0.05) for pelleted earthworm diet groups followed by whole earthworm and earthworm custard diet fed groups.05) compared to whole earthworm (D-1) and earthworm custard (D-2) fed groups (Table 4). protein efficiency ratio. Results  In the present study.8 ± 1.21 ± 0. Values are the means of three replicates ± standard error (SE) for each experimental diet.18 ± 0. Whole body composition of L.3 ± 0.17 ± 0.1080/23311932.94 ± 0.93 ± 0.8±0. Table 5.58 ± 0.05 c 2. between the whole earthworm diet and earthworm custard diet fed groups.75 ± 0.2016. Mohanta et al.03a 0. statistical package used for the analysis of data was PC-SAS programme for Windows. 3.12 (SAS.19  ± 0.85 ± 0.07a Weight gain (g) 1. The growth performance of L. The fish fed pelleted earthworm diet (D-3) had significantly higher (p < 0.34 ± 0.05b 0.3b Total ash 102.09c 18.30 ± 0. there was no mortality or abnormality of fish found in any of the dietary treat- ments.6 ± 0.21 ± 0.65 ± 0.07b 2. 1996).doi.6 ± 0. Page 7 of 13 . However.69a Downloaded by [157.8b 654.3 ± 0.7a Ether extract 141.42 ± 0.3a 748 ± 8.05) weight gain.15b 10. rohita advanced fry fed different experimental diets after 35 days of culture Parameters D-1 (Whole D-2 (Earthworm D-3 (Pelleted earthworm diet) custard diet) earthworm diet) Initial weight (g) 0. in contrary to the protein.

Guerrero. growth factor. Ugwumba. Liew.. Ng. 2003. 1995. The higher body lipid content might have re- sulted in lower body protein content as there is always an inverse relationship between the protein and lipid contents in animal tissue. turkey meal (Muzinic. Ang. Ugwumba. Istiqomah et al. & Webster. 2008. Dong. 2004. 1997). the protein and lipid contents of the earthworm are species specific. Nandeesha. Wang.doi. Ugwumba. Li. & Mukhopadhyay. 2001). 2003. phytates. 2008. In the present study..1080/23311932. Whiteman & Gatlin. Hardy. fermented fish silage (Fagbenro & Jauncey. 2001). 2006. 2008. garden snail meal (Sogbesan. 2008a). The hard cuticle in the earthworm contains the chitin. 2008. mimosine. fermented fish offal meal (Mondal. 2005). Sogbesan & Madu. Barik.. 1997).1138594 4. Babbitt. fisheries by-catch and fish processing by-products (Goddard et al. vitamins con- tents. Keshavanath. 2006.. Medina et al. 1988a. glycosides.. & Chunyang. poultry by-product (Yigit et al. saponegin. and attractant properties and therefore. Sulochona. 1987) and therefore. & Mustafa. Thompson et al.. Moreover. it is difficult to compare the nutrient composition of the earthworm found in the present study and the earlier reports. & Gatlin III. worm meal (Ng et al. Lihui. 2002). 1983).org/10. it may be due to the presence of more chitin that is derived from cuticle when earthworm was incorporated at higher levels (100% in D-1 and 60% in D-2) in the diets. 2009. The earthworm (E. most widely used protein ingredients in aquafeed (Goddard et al. (2001) reported the growth depression Page 8 of 13 . 1995). & Hardy. the increasing cost of high-quality fish meal required for aquafeed and the declining stocks of fish from capture fishery and competition for feed in animal husbandry compelled the fish nutritionists around the globe to investigate and identify the novel and renewable alternative non-conventional protein source for the continued expansion and sustainability of aquaculture industry (Sales & Janssens. Stafford & Tacon. Ugwumba. Gaur. 2006). 2005. 2005). and linamarin to mention a few despite their nutrient values and low cost implications (New. Many researchers have Downloaded by [157. & Singh. silkworm pupae (Edwards & Niederer. 2005).. 2007). 2001).2016. & Guroy.8% fiber (on dry weight basis).10] at 07:06 19 September 2017 reported the use of several non-conventional animal protein sources such as earthworm (Kostecka and Paczka. 1987. & Okunola. Rathbone. & Madu. The whole body protein and lipid contents of earthworm used in the present study were 52% and 18%. respectively. Mohanta et al. Nandeesha et al. Pereira & Gomes. slaughter house waste meal (Singh. Sogbesan & Madu. the earthworm used in the present study contains 7.. Metts. 2001. the animal protein source is preferred over the plant protein in formulating the fish feed. 1983. & Gatlin III. 1994). Hardy & Barrows. 1984.. Reinecke & Alberts. Kaviraj. Tacon et al. Cogent Food & Agriculture (2016). 2008. Reinecke & Alberts. co-dried fish silage (Goddard & Perret. 1990). & Madu.. 2003. cyanoglycosides. Discussion Fish meal is considered as the best protein source due to its balanced amino acids. Varghese. Tacon. Dasgupta. Moreover. maggot meal (Sogbesan. Subramanian. The utilization of non-conventional feed stuffs of plant origin had been limited as a results of the presence of alkaloids. Sogbesan & Madu. 2006. Xianchun. As we do not know the culture environment of the earth- worm as reported by the earlier researchers. & Shethy. But fish meal represents a finite fishery resource and will not be able to supply the aquaculture industry with a continuous source of cheap protein indefinitely (Ng. Ng et al. The growth and dietary performance of fish fed whole frozen earthworm (D-1) and earthworm-based custard (D-2) was not encouraging. 1983. & Korikanthimath. Shapawi. tuna by-product meal (Tekinay. The crude protein content of earthworm was lower than many of the earlier reported values (Guerrero. Ajuonu. oxalic acids. the culture environment (nutrient/medium) plays a great role in determining the nutrient composition of earthworm. 2009). protease inhibitors. 1987. Sogbesan & Ugwumba.48.. 2005. But the whole body lipid content of 18% is found to be significantly higher than the earlier reported values (Dynes.12. Similar to our observations. foetida) meal has high protein content and the amino acid compositions are close to fish meal and hen egg (Medina et al. 1988. Deveciler. which mostly repre- sent its chitin content. Although we have not measured the chitin contents in the diets. 2008. Thompson. Srikanth. 2003. Hardy.. 2013). earthworm was used in formulating experimental diets and the diets were fed to rohu advanced fry to elucidate the poten- tiality of earthworm as a dietary protein source. 2011). 2: 1138594 http://dx. 2007). termite meal (Sogbesan & Ugwumba. Sealey. Chitin is a polymer of glucosamine and is insoluble in common solvents. & Wong. Zhenjun et al. heamatoglutinins. Again. 2008b). Zhenjun. and surimi by-product meal (Mohanta. palatability.

Nandeesha. (1988) tried to replace fish meal partially or completely with dried worm meal (Eudrilus eugeniae) in the culture of common carp and found that the diet where the fish meal is partially replaced by earthworm meal (incorporating 5% sardine oil) gave best results than the diets where the fish meal is completely replaced by earthworm meal or a diet prepared by using fish meal as sole protein source without any worm meal (control). 1990. Nandeesha et al. foetida. The FCR of 1. but there was decline in fish performance at higher re- placement levels of 50 and 100%. for which the growth is significantly Downloaded by [157. Shiau and Yu (1999) reported that tilapia Oreochromis niloticus × O. survival was higher in former (75. in which herring meal was used as the sole source of dietary protein. Stafford and Tacon (1984) reported that the growth and feed utilization efficiency of rainbow trout was not affected when the herring meal protein is replaced by earthworm (Dendrodrilus subrubicundus) meal at 10%. (1983) reported a slightly lower growth response in rainbow trout when worm meal (E. According to Edwards and Niederer (1988). with 25–50% of dietary protein could be supplied from worm meal. the diet D-3. 1994. 2006). and cystine in earthworm as reported by Tacon and Jackson (1985) and Pereira and Gomes (1995). et al.55.66%).50.12.52–3.1138594 and poor feed and protein utilization in cat fish fed high levels of meal worm or solely on meal worms due to presence of chitin in the meal worm. foetida in the diet of rainbow trout Salmo gairdneri and reported that there was no adverse effect on the growth performance or feed utilization efficiency of fish fed diets containing low levels of earthworm meal. rohita (1. foetida) was used to replace 50% dietary her- ring meal protein compared to fish fed control diet. & Hasan. In the present study. and krill meal (5%).58 obtained in the present study in fish fed diets D-3 containing dried earthworm as main protein source is similar or even better to the earlier researchers who used different non-con- ventional dietary protein sources such as fisheries by-catch and processing waste for tilapia (1. we observed best growth and nutrient utilization in fish fed pelleted earthworm diet (D-3) containing 40% earthworm as major protein source. Gangadhara. Mohanta et al.21–1... Srikanth. Srikanth. Akiyama et al. Hossain. 2000).1080/23311932. foetida worm meal than the fish meal-based diet.org/10.35.2016. foetida) biomass resulted in significantly increased brood number and also produced twice the off-spring than the fish fed a diet without earthworm. (1983) reported that the rainbow trout fed 100% worm meal (E. worm meal is able to substitute fish meal for monogastric animals and fish. silkworm pupae in carps (1.05) than other two diets. 2: 1138594 http://dx. (1984) reported that the chum salmon Oncorhynchus keta swim up fry fed fish meal diets supplemented with earthworm powder (5%) showed the best growth performance and feed efficiency than fish fed fish meal diets supplemented with silkworm pupae powder (5%). 2008). aureaus fed diets with chitin as low as 2% exhibited depressed growth and feed effi- ciency. Nandeesha. Basavaraja.75%) than the later (66. Nandeesha.. Ganesh et al. Bhuiyan. Tacon et al. 1988a. Cogent Food & Agriculture (2016). 1991). garden snail meal in Clarias gariepinus (1. & Keshavanath. et al.48. 1988. Goddard et al.. dried beef liver (5%). slaughter house waste in L. about 25% of the dietary protein had supplied by earthworm meal.89–2. In the present study. gave higher growth rates in fish fed these diets compared to control diet without any worm meal (Velasquez et al. Further. Experimental results of Keshavappa et al. In contrast. Mahata. Another reason for low growth and nutrient utilization in fish fed solely (D-1) or higher levels (D-2) of earthworm in the diets may be due to deficiency in certain amino acid like lysine. Sogbesan et al. Kostecka and Paczka (2006) reported that the aquarium fish Poecilia reticulata fed earthworm (E.34– 1.. Tacon et al. Varghese. (2003) observed better growth and nutrient utilization in carp (Cirrhinus mrigala) fed diet containing E. (1989) showed no difference in weight gains in carp (Catla catla) fry fed 30% inclu- sion of earthworm meal compared to the 30% inclusion of fish meal. Worm meal obtained from E. Singh Page 9 of 13 .. Stafford and Tacon (1985) evaluated the dried earthworm meal derived from E. Edwards & Niederer.44. foetida) protein in the form of frozen slices did not yield any encouraging growth and dietary performance which is in agreement with our study. Pereira and Gomes (1995) also reported that the growth rate and feed utilization efficiency affected adversely when the diets containing high level of frozen worms were fed to rainbow trout. Similar to our results. methio- nine. Zaher. Varghese.10] at 07:06 19 September 2017 better (p < 0. when used to replace 25 and 50% of the fish meal compo- nent in the diets for rainbow trout.doi.

3–1.05) be- tween the initial and final fish.99–1. 2007). Thompson et al..71–1.48 in L. Chrysops  ×  M.7–23. The PER of 1.1. 2008). Similar to protein retention. gariepinus fed garden snail meal-based diets (Sogbesan et al. 1.3% reported by Mondal et al. 2006).07 reported in P.. 1. 0. 2005). & Sahu. 0. 1992). 0.36 in H. 2001). 2009 for rainbow trout with tuna by-product.7 in Cromileptes altivelis fed poultry by-prod- uct meal (Shapawi et al. Singh et al. mykiss fed tuna by-product meal (Tekinay et al. Mohanta et al. saxatilis (1. 0. 2011). Mondal et al. Cogent Food & Agriculture (2016). 1994.86–3.2016. 2008). Muzinic et al.48. The significant higher growth rate and comparatively more whole body energy in D-3 group of fish resulted more energy gain than other two groups... Tekinay et al.65.70–2. gonionotus and common carp Cyprinus carpio fed silkworm pupae- based diet (Mahata et al. The negative correlation between whole body protein and lipid contents was reported in many fish species (Hafedh.73– 2.75. 2009).1138594 et al.. The SGR values obtained in the present study is compared with reported values of fish fed diets containing various non-conventional animal protein sources and it was found that the SGR value of 4..58–1. 2006). 2008.7–3.. the energy retention was also found to be signifi- cantly better in D-3 fed group than the D-1 and D-2 fed groups.87... The higher SGR obtained in the present study than many of the other researchers as mentioned here could be due to compara- tively more weight gain of fish in a shorter rearing period of 35 days..31–31.. protein.1080/23311932. Muzinic et al.7. rohita with slaughter house waste.6–0.05. but lower lipid and ash contents. there was a significant variation in whole body protein... 0.80 by Shapawi et al. The protein retention of 23..45 in Psetta maeotica fed poultry by product meal diets (Yigit et al. saxatilis (1. Mondal et al. 2009) and 1. 1. 2: 1138594 http://dx.. 0. 2007 for sunshine bass with turkey meal. 2011).6–1. Thompson et al.. Mohanty. 2005 for L. chrysops × M.. 0.. 2006..34 in L. 1998). Page 10 of 13 . bata fed fermented fish offal meal (Mondal et al. altivelis with poultry by-product meal. 1990). The fish fed D-3 diet had significantly higher whole body protein content. The higher growth rate and whole body protein and also the proportionately lower dietary protein fed in relation to weight gain in this group of fish resulted significantly higher protein retention than D-1 and D-2 groups of fish. turkey meal in M.21 obtained in diet T-3 (earthworm meal-based dry pelleted diet) is either comparable or better than the 0. altivelis with poultry by-product meal-based diets. Oncorhynchus mykiss (1.. 1. (2011) for L..84–3.12... 1.2–1.1 in Oreochromis niloticus fed fisheries by-catch and processing meal waste-based diets (Goddard et al. 0. 2007). The whole body moisture. 2005). ether extract and ash contents. tuna-by product meal in rainbow trout.98 in Heterobranchus longifilis fed earth- worm meal-based diets (Sogbesan et al. Tekinay et al... 3.26 obtained in D-3 is comparable to the PER reported by different authors using vari- ous non-conventional protein sources in the diet of fish (1.. 2008). Shapawi et al. lipid. and ash contents in the present study are in the same ranges as reported by earlier researchers for other fish species fed with different non-conventional protein sources (Goddard et al. and fermented fish offal in Labeo bata (1.51–0.doi. 2006. 1999. 2007).25. Mondal et al. The higher whole body protein content in D-3 is reflected as more weight gain in this group of fish. This may be due to more energy gain in fish fed diet D-3 in relation to dietary energy fed through diet.20–1. Mondal et al. rohita (1.0% found in fish fed diet D-3 in the present study is similar to the 14.05 in M.7 in O.. poultry by-product meal in Morone chrysops  ×  M..2 in Clarias gariepinus fed mealworm-based diets (Ng et al. fermented fish offal in Heteropneustes fossilis (1. Nandeesha et al.. blood meal in L.19–1. saxatilis fed turkey meal-based Downloaded by [157.59–0. 2. 2011 for Labeo bata with ferment- ed fish offal meal). 2006). Mohanta. 2007 for C.4–1.9. rohita fed offal meal based diets (Khan & Jafri.10] at 07:06 19 September 2017 diets (Muzinic et al..72. Thompson et al. 2011.7. Saha & Ray. The whole body protein and lipid are inversely related.99 in L. Although the whole body moisture and energy contents did not vary significantly (p > 0. rohita fed slaughter house waste meal (Singh et al. 2008).65–2. (2007) for C. 2006).54–1.62–0. bata fed fermented fish offal-based diets and 18.75–1.5.org/10. Rawles et al. Jena.71 in C.3–1. 2006).05–1. fossilis fed fermented fish offal-based diets (Mondal et al.

India for extending all the infrastructure facilities http://dx. L.. 181–184. Earthworm Keshavappa.doi.org/10. Istiqomah.org/10. W. W. (2002). http://dx. (1975).. Institute of Terrestrial Ecology.. T.03/085. D. Earthworm meal for fish feed formulation and Funding its influence on growth of mrigal fingerlings.1138594 From the present study. (1999). Goa 403402. (Eudrillus euginae) multiplication through variable Evaluation of three animal based feeds for rearing of substrates.org/10. Y. A. E-mail: manjunathpi@rediffmail. E.doi. F.. Competing interests http://dx.1111/j. J. G. Tropical Animal Agriculture. European Journal of Soil Biology. Possible use of earthworm Edwards.. G. In J. R.12. Aquaculture Research. Aug 30–Sep 4). nutrient Nutritional value of fisheries by-catch and by-product Page 11 of 13 . VA: Author. Devaraj. III (2005). The culture and use of ORCID ID: http://orcid. Earthworms–Technology information Khan. New York. Das. 118. by-catch and by-product meals as protein sources for Supplementation of various meals to fish meal diet for rainbow trout Oncorhynchus mykiss. & Perret. (2009)... Mohan. Halver & R.029 management (pp. Journal of Aquaculture.doi.org/0000-0002-4476-8594 Peronya excavatus as a protein resource in the Phillippines Sankaran Subramanian1 (250 p. X. J. In Proceedings of the National Symposium on http://dx.. R. A. Wang. Y. 2. The fatty acid fry. use in aquafeeds. E. Fagbenro.. T. A. In C.. M.. (2008). 32–340. Subha..). Damayanti. M. D. Ela.). M. (1989). V. Journal of The research was supported by Indian Council of Ecobiology. New Delhi. & Seenappa. III (2004). Labeo rohita (Ham.org/10.1080/23311932. Cogent Food & Science of Food and Agriculture. (1984). (1979). Downloaded by [157. Odisha. G.ejsobi. http://dx.00343.org/10. Oreochromis niloticus.org/10. DC: Author. (1992). Al-Shagaa.11.).x Guerrero.15. S. Sankaran Subramanian & composition of the lipids of earthworms. & Gatlin. Hafedh. W. Water stability. 30. 143–144). (1983). & Czochanska. Fish Source: Authors. Arlington.07. Mohanta et al. & Ali. Cogent Food & Agriculture (2016). India. Central Institute of Chapman and Hall. 143–153. Cite this article as: Potential of earthworm (Eisenia foetida) http://dx. & Jauncey. O. it is concluded that the earthworm could be used as an ideal alternate protein source for formulating the diet of L. Kausalyaganga. 1. R.10] at 07:06 19 September 2017 Kedar Nath Mohanta1. P.. Institute of Veeratayya Sidweerayya Korikanthimath1 Terrestrial Ecology. K. (2006).. & Das.doi. 277–283. Hardy. 37. 217–222. 56–62. Journal of the Indonesian Chemists (Vol. Journal of the Veeratayya Sidweerayya Korikanthimath. Hague: Academic Publishing.48.. D.1365-2109. VA.2 39. S231–S233. (1981. Association of Official Analytical Chemists.. 42. nutrition (3rd ed. P.. J. 169–180).1046/j. 36. A. & Julendra.doi. S. Dynes.1111/anu. Kedar Nath Mohanta. 309–313). 32. & Nose.issue-5 Freshwater Aquaculture (pp. rohita advanced fry and the pelleted earthworm diet is better utilized by rohu for its growth and nutritional gains as compared to whole earthworm and earthworm custard diets. P.... ICAR Research Complex for Goa. R. excavatus as protein resource in the Philippines. 253–257. Replacement of fish meal with to enable the development of earthworm production offal meal in formulated diets for the carp fingerlings (Publication No.). S. Z. G. F. & Pączka. Ministry of Agriculture. (2005). T. 1. 1102 p. (1995). for Goa. Edwards & E. 14.. C. Hilton. (1990). R. ry E-mail: knmohanta@gmail. Arlington. In J. Y. M. (1989). Bhubaneswar. K. Goddard. 3. 505–600). Aquaculture. R. Hardy (Eds.1365-2109.doi.01906.anifeedsci. Fisheries by-catch and processing waste meals as ingredients in diets for Author details Nile tilapia. (1988).1007/978-94-009-5965-1 751002. M. Neuhauser (Eds. Earthworms in waste and environmental http://dx. London: 2 Fish Nutrition and Physiology Division.. 385–393. catla fry. 961–971. 26.1016/j. Co-drying fish silage for Government of India. A. W. & Niederer.org/10. 23 September. methods of analysis of the Association of Official Analytical Oecologia. 518–525. 2: 1138594 http://dx. Murai. & Barrows. Chakrabarty. R. NY: Academic Press. Agricultural Research (ICAR). A. ICAR Research Complex fish silage diets. Potential of freeze-dried worm meal as American Public Health Association.doi. D. D. 2: 1138594. Acknowledgements leaching and nutritional properties of moist fermented The authors are thankful to Director. R. Diet formulation and Cover image manufacturing. J. Official Amino acid profile of earthworm meal (Lumbricus methods of analysis of the Association of Official Analytical rubellius) for animal feed stuff. F. pp. & Gatlin..2006. Washington.1016/0144-8609(94)P4432-B needed for the experiment. Fisheries Akiyama. 393–400. K. Freshwater Aquaculture. 14th ed..com http://dx. Ganesh. Dorwin Centenary Symposium On Earthworm E-mail: subra550@yahoo.x as dietary protein source for rohu (Labeo rohita) advanced Hansen. Li.. The production and Eisenia fetida (Sav. Kostecka. Satchell (Ed.2016.1016/j.2004. pp. (1983).1016/0044-8486(84)90154-6 Hartenstein.2008. & Kaplan. A. 15. H. India. Old Goa. 513–516. Agriculture (2016). Goddard.com Guerrero.doi.. E. Aquaculture Society.doi.).). The culture and use of Perionxy 1 Fish and Fishery Science. Neuhauser.1002/(ISSN)1097-0010 Hardy. S. Standard methods a replacement for fish meal in trout diet formulations. Aquaculture Nutrition. Association of Official Analytical Chemists (1990). Aquaculture.).. D. 34. processing of earthworm protein. Chemists (Vol.org/10. for examination of water and wastewater (17th ed. T. Bhubaneswar http://dx.. A. A.. Journal of World chum salmon fry.. Citation information Aquaculture Research. Kingston: RIRDC. References Hardy. R.).. 14th ed. S. Oreochromis niloticus L. W. L. Hirasawa. & Jafri... Sofyan. K. 337–342. 1102 p. E.. Animal Feed Science and Technology. (2009). & Vijayalakshmi. D. K. W. Earthworm ecology (pp. M.2009. 1–33). (2003).) biomass for breeding aquarium fish. Sealey.org/10. (2003).doi.1999. Official Reproductive potential of earthworm Eisenia foetida.com Ecology.004 The authors declare no competing interest.. Aquacultural Engineering. M.org/10. S. Effects of dietary protein on growth and body composition of Nile tilapia. 43.

16. J. deboned fish wastes. C. 71–81. Effect of protein levels on growth Influence of earthworm meal on the growth and flesh and digestibility in the Indian major carp. altivelis. N. (1988).x 6. Turkish Journal of Fisheries and A manual on the preparation and presentation of Aquatic Science.x Aquaculture. K.. F. (1990)... M. A. K. & the protein ingredient. Singh. Cogent Food & Agriculture (2016).doi.549783 rohita).doi. K. chrysops ♀×M. Replacement of fish meal protein by surimi by. R.1080/23311932. Srikanth. J. 143–152. Reinecke. W. A.1111/j. Aquaculture.org/10. D. Washington.014 (Eds..2006.. Varghese. NC: SAS Institute. S... 4. Freeman.. S.doi. Srikanth. Srikanth. (1987). Cyprinus carpio fed with high levels of Sogbesan. Varghese. D. B.01237.48... Varghese. Keshavanath. C.doi. S.1365-2095. Journal of Aquaculture in the Tropics. Gaur.1016/j.. M. Eudrilidae) meal as protein feedstuff in diets for http://dx.-K. & A. http://dx.aquliv. Shukla. http://dx. (1995). & Alberts. Riche. 14. Mahata. & Ray. M. N. Mondal. Tydskrif Vir.doi. 23–31. 17–23.conventional animal protein 235–242. J.-L.. & Ugwumba. Kaviraj. niloticus×O... A. W. Journal of Animal Physiology and Oligocheata) as potential source of protein for animal Animal Nutrition. of proteins from Eisenia foetida. practices in Nigeria. (2003). Journal of Aquaculture in Tropics.2007.. M Bouwmans http://dx. S.1111/anu.org/10. Page 12 of 13 . C. 26.. Valenciennes 1840 (Teleostei. & Madu. NRC (1993). Mondal. P. J. Biological Wastes. earthworm. A. J. feed. A. T.2006. Influence of fish meal with poultry by-product meal in diets of silkworm pupae based diets on grown organoleptic formulated for the humpback grouper. S. O.010 Pereira. 7. Liew. Mohanta. 39. (1998). Bhuiyan. Shethy. 77–85. L. J. M... W. http://dx. (2005).org/10. K.. K. (1987). Jena. 939–941. Evaluation of earthworm silkworm-pupae in diets on the growth of common carp. 533–540. 8. Clausen.issue-1 Agricultural Immunology.1439-0396. (2008a). 10–19.. K. Evaluation of silkworm pupae Performance of juvenile coho salmon Oncorhynchus as dietary protein source for Thai sharpunti Puntius kisutch fed diets containing meals from fish wastes. Cova. rohita (Hamilton). D. P. Effects of non-defatted Sogbesan. & Hardy.2011.(1988.12. & Janssens. Ang.. PC-SAS Programme for Windows release v6. K. 8. gonionotus.doi. & Gomes. P. 2: 1138594 http://dx.12. 95.. & Ugwumba. Subramanian. M. 1–14.doi. S. 118–126.2003. J. Nutritional p. gariepinus. K. Potential meal as animal protein supplements in the diets of of mealworm (Tenebrio molitor) as an alternative protein Heterobranchus longifilis (Valenciennes. (2008b). K. Growth response and flesh quality Journal of Environmental Sciences. & Mukhopadhyay. M.. F. Aquaculture. R. O. P. & Varghese. Rawles. Y. G.. N. Asian Fisheries Science. SAS. (2003).2001. T. Nandeesha. A.aquaculture. (2001). & Yu. Rome. 485–496.org/10. (1986). Natuurwetenskap en Tengnologie. 179. A. Mohanta. Labeo rohita quality of common carp. G. N.. W. A.org/10. J..1016/j. A. R. Mohanty. C. 236. & Madu. P. J.doi.. (1994). Research Keshavanath. Aquaculture International.. N.06. G. C. (2000). A. K. (2002).. V. or skin-and-bone by-product as Medina. K. 273. Muzinic. A. A.doi.doi. Nutrient requirements of fish (114 p. P. K.org/10. Nutritional non-defatted silkworm pupae. P. 21–29.001 in tanks. R. Protein Evaluation of fermented fish offal in the formulated requirement of carps. International Journal of Agriculture and Biology.. aureus. Oreochromis on Aquaculture Organized by IFS Malang (pp. Nandeesha. J. Proceedings of the Asian Seminar and chitosan depresses growth in tilapia. A. 13. 23. Webster. Feed and feeding of fish and shrimp. & 277–284.-P. 36–42. Ray. A. T.2004.1007/BF03179363 replacement of fishmeal by fermented fish-offal meal in Saha. Aquaculture Nutrition. A. C.. 1840) fingerlings. Clariidae) fingerlings under laboratory condition. Clarias Turkish Journal of Fisheries and Aquatic Science.org/10.. Nandeesha. R.doi. Ng.. 377–389. D. L.. O.). DC: National Research Council. products in carp diets: Evaluation of poultry litter and Journal of Applied Aquaculture.1016/S0044-8486(99)00177-5 Nandeesha. & Kale. Keshavanath.1355-557x. M.1016/j. A. Dietary supplementation of chitin techniques and nutrition. & Davis. (2007).x Sogbesan. (2006). K.. & Wong. S. N.doi. M. Biological Wastes. 159–164.. T. N. Vidna. Catla catla (Hamilton) and Labeo diet of the freshwater catfish Heteropneustes fossilis. & Sahu. & Mukhopadhyay. of common carp... 149–157. Oligocheata: Cyprinus carpio. Worms. 15. (2008).1080/10454438. A. R. O. Basavaraja. 211–220). Gangadhara. M. Proceedings: Animal Sciences. K.... Cromileptes quality and biochemical composition of catla-rohu hybrid.00024. Food and http://dx. K. P.2016. fingerlings. H. S. M. http://dx.. A.1016/0269-7483(90)90118-C Heterobranchus longifilis. Aquaculture Nutrition. http://dx. T. G. K.). Aquaculture research in Asia.. & Korikanthimath. Keshavanath.2001. Varghese. C. (2011). A. G. 259. A. L. 443–1449. 41–50.09...-K. M.. S. Dong. Carlos. compound feeds for shrimp and fish in aquaculture (275 Sogbesan.. Bano. S. P.org/10. (Hyperiodrilus euryaulos. (1999). S. T.. A.. November 14–18). N. S. J. (Hamilton) using slaughter house waste as the protein http://dx. 97.doi. P.A. 251–263.. V. 33. S. 189–198.05. Growth of rainbow trout Lieberman. & Mustafa... Management Shiau. C.doi.... J.aquaculture. Zonneveld. Metts. Aquaculture Research. B. Hossain. K. Sulochona. S. G.-P. (2006). 1914.. (2008). Aquaculture Research. D. FAO ADCP/REP/87/26. 103–107. E. Basavaraja... Use of turkey meal as partial and Sales. 32.1016/0269-7483(88)90165-6 source. The chemical and amino product protein in the diet of blue gourami Trichogaster acid composition of the compost worm (Eisenia foetida Downloaded by [157.).org/10. National Academy Press... K. M.. Aquatic Living Resources. values of some non.. S.12. (2008).issue-1 Cary. A. Puntius gonionotus meal in commercial diets for hybrid striped bass (Morone fingerlings. Incorporation of Animal by- the formulation of diet for indian minor carp Labeo bata. evaluation of termite (Macrotermes subhyalinus) Ng. Kaviraj.doi. F. K. M. Dasgupta. A. Y. 12...org/10. Huisman. 273–280. Evaluation of poultry by-product Protein requirement of silver barb.00514. Renukaradhya. 9. 2.2011. Babbitt.10] at 07:06 19 September 2017 trichopterus fingerlings.1016/j. & Hasan. A.053 (2013). Barik. Replacement P. Ugwumba. feedstuffs used as fishmeal supplement in aquaculture New.org/10.02.32.. Shapawi. Journal of the World Aquaculture Toress. S.. M. goat blood meal as dietary protein source for rohu (Labeo http://dx. http://dx. G. (2001).-W. after chemical Worm Digest. Gaylord. Mohanta et al. Thompson. A. & Singh. Das. 439–446. treatment. saxatilis ♂) in recirculated tank production. L. 11–18.. beautiful worms. Aquaculture.1111/j. In E. O. H.. A... http://dx. 3. 32.org/10.aquaculture. sunshine bass (Morone chrysops × Morone saxatilis) grown http://dx. Zaher.1046/j. R.1111/jwas. Ajuonu. Rathbone. Immunology and chemical analysis Society.org/10... C. P. (1996). 13.2007. N. Partial http://dx. Webb. K. C. Pujic. Puduc. International fed a diet supplemented with earthworms. P.org/10.1138594 meals in the diet of red drum (Sciaenops ocellatus).org/10. T. Nutrient requirements of total replacement of fish meal in practical diets for ornamental fish. K. source in practical diets for African catfish. K.

. The licensor cannot revoke these freedoms as long as you follow the license terms. Substituting fish meal with poultry by-product Academic Press.doi. A. Evaluation of resources (FAO of United Nations. 51–55. (1985). A. Dendrodrilus subrubicundus. 35. (1991). Ergun.issue-16 practical fish feeds. E. & Tsukamoto. A. The use of earthworms http://dx. Earthworms in Waste size and stage structure on lumbricid Eisenia foetida and Environmental Management (pp.doi. 36.. (1988). D. A.. C.. fetida) in diets for rainbow trout. & Okunola. W. Hague: population in a field compost and its practical application SPB Academic Publishing. North American Journal Stafford.. C. A.. & Edwards. Fisheries Circular fisheries by-catch and by-product meals in diets for red No. Xianchun. transform. S. & Jackson. Utilization of 1572–1580.org/10.10] at 07:06 19 September 2017 Stafford. G.org/10. 187–199. México. A. A. G. 35(1).. Revue D Tacon. C. 5. M. G. Under the following terms: Attribution — You must give appropriate credit._E. (2005). 13. Bell Yigit. M. Y. preliminary investigation of the nutritive value of http://dx. C. J. & Madu. S. 2: 1138594 http://dx. K. as the decomposer of organic waste matter. J. G. A. O. the earthworm. J. 35 p. (1976).36. In C. S. Muzinic.org/10..1 domestic sewage. E. Ibañez. M. International. (2006). 351–359. 221–236.. & Oyarzun. Stafford.1017/S000335610000605X as a food for rainbow trout Salmo gairdneri. 193–208). L.2016.org/10. E. species.1016/0141-4607(84)90084-2 growth of Clarias gariepinus (Burchell) fingerlings. Journal of Fisheries Sogbesan. Page 13 of 13 . H. B. preliminary investigation of the nutritive value of http://dx. A. 69. (2007).. J. & Tacon. (2001). G. a replacement for menhaden fish meal in practical diets 1999–2003.. In C. (1984). Nigerian Stafford. African Journal of Biotechnology.doi. (1985)..12. Effect of dietary concrete tanks. Dasgupta.1111/anu. R. & Tacon. Tacon. A. 119–122. (2009). Tacon. Journal of Industrial and Scientific tuna by-products on feed intake and utilization of Research. L. conventional and unconventional protein sources in http://dx. A. J.881. Zhenjun. No additional restrictions You may not apply legal terms or technological measures that legally restrict others from doing anything the license permits. M. D. S. Koshio. & Brady. Aquaculture Research.org/10. A. A Food and Nutrition.. rainbow trout Oncorhynchus mykiss.issue-5 three terrestrial lumbricid worms for rainbow trout. Mohanta et al. A. for sunshine bass grown in cages... Ugwumba. A. (1983). Rome.. Nutritive potentials and utilization of garden snail Thompson. & Guroy. You are free to: Share — copy and redistribute the material in any medium or format Adapt — remix. 8–12. (Limicolaria aurora) meat meal in the diet of Clarias Webster. The Nutritive evaluation Journal of Science.doi. Nutrition and feeding in fish (pp..0 license. London: B. provide a link to the license. 35. Metts. meal in diets for black Sea turbot Psetta maeotica. You may do so in any reasonable manner. 4. grown on http://dx. Downloaded by [157. A. 187–199. 141–146. Cost benefits of maggot meal as supplemented Aquaculture. Lihui.doi.org/10. Earthworm as a potential protein resource.2006. A low levels in production diets for rainbow trout (Salmon note on the nutritional evaluation of worm meal (Eisenia gairdineri). A. O. Turker.. T. Feed ingredients for carnivorous fish Ecologie Et De Biologie Du Sol.Edwards& E.. A.1138594 T. even commercially. (1982).1997. J. Nutritive value of of Aquaculture.Neuhauser (Eds.. C. Cowey. in trout diets. A. FIRI/C881. 16. 9.1080/23311932. Animal Production. A. 119–145). M. A. Published by Taylor & Francis. A.. 3.1111/are. I. & Tacon. A.doi. J. Use of Turkey meal as gariepinus fingerlings. O. A.9991517 three terrestrial lumbricid worms for rainbow trout. 213–222.org/10. 340–347. Seasonal changes in A.. S. G.)..org/10. G. A.. Ugwumba. Ecology of Tacon.. Stafford. drum Sciaenops ocellatus L. J. & Chunyang. G.1577/A07-007. (Eds. 53. E.. Cogent Food & Agriculture (2016). Mackie. Alternatives to fishmeal and other fishery Whiteman.doi. Fisheries Management.12. Aquaculture and. & Edwards. A. 12. & Karaali. Deveciler.).doi. & J. & Gatlin. Agricultural Wastes.48. Aquaculture. but not in any way that suggests the licensor endorses you or your use. This open access article is distributed under a Creative Commons Attribution (CC-BY) 4. F. (1994). A. 36.. J. A. A. and build upon the material for any purpose.. A Aquaculture Nutrition. and indicate if changes were made. L... D. (1997).. Ugwumba. Utilization of live maggot as supplementary feed on the http://dx. © 2016 Instituto Tecnológico de Durango. Herrera.1016/0044-8486(83)90090-X gariepinus (Pisces-Clariidae) hybrid fingerlings in outdoor Tekinay. Watanabe. J. S. S. E. (2006).2005. feed in the diets of Heterobranchus longifilis x Clarias http://dx. 1–7.).1080/03670244.. L. of dried earthworm meal (Eisenia foetida) included at Velasquez. 249–266. Erdem. (2005). A. K.