Utilization of earthworms (Perionyx excavatus) as a protein source for growing fingerling marble goby (Oxyeleotris marmoratus) and tra catfish (Pangasius hypophthalmus)
 

Nguyen Huu Yen Nhi

Faculty of Agricultural and Natural resource, An Giang University,
Long Xuyen City, Vietnam
nhynhi@agu.edu.vn

Literature review

Biological characteristics and feeding behavior of two fish species

Marble goby (Oxyeleotris marmoratus)

According to the fish-base website, Marble goby, goby or Marbled sleeper goby are common names for the carnivorous fish Oxyeleotris marmoratus or Oxyeleotris marmorata (Bleeker, 1852) which is a member of the family Eleotridae. This species is one of the largest goby in the world and grows up to 50 cm in total length and reaches maturity at approximately 7 cm (Tan and Lam 1973). Marble goby is found in natural waters, cages, ponds and coves in Vietnam, Cambodia, Thailand, Indonesia, Singapore and Malaysia (Cheah et al 1994; Vu Cam Luong et al 2005). The young stage is free-swimming and later on has bottom-dwelling habits (Seenoo et al 1994).

Marble goby have an elongated body and no lateral line. They are dark brown on the dorsal side and pale brown on the ventral side. There are long dark blotches on the body. The body color is variable and depends on the environment of the habitat bottom and lighting. The fins have no spines and have black or dusty bands. This species is sluggish and prefers to spend most of the time buried in the habitat substrate with eyes protruding to ambush its prey (Kelvin and Peter 2002).

In nature, Marble goby is a carnivorous fish, considered to be a motionless species that ambush their prey.  It usually eats at the bottom and preys on small fish, insects and zoo-benthos, like crustaceans, mollusks which live at the bottom. It seems that the fingerlings and adults of wild Marble goby feed mainly on small fish, small freshwater prawns and benthos. The proportion of feed found in the stomach increases with size of fish size as well as with seasonal availability of prey (Vu Cam Luong et al 2005). The same result was also found by Nguyen Phu Hoa and Yang Yi (2007), in that the number of small shrimp eaten by big Marble goby was much more than in the small Marble goby.

Until recently, Marble goby culture systems did not rely on artificial pelleted feeds. Feeding of this species is still predominantly traditional, usually with trash fish, rice bran, poultry slaughter house by-products or a combination of these (Edwards and Allan 2004; Suchart et al 2005).

Marble goby fry reared in earthen ponds have had a low survival rate (25 -50 %) (Panu et al 1984). The cause of fry mortality was mainly through predators, stress and improper collection.  The Marble goby have a habit of hiding in muddy water, so it makes fry collection difficult (Rakbankerd 2005). However, juveniles seem to grow faster when supplementary feeds containing high protein animal sources and natural foods are presented in sufficient quantity. Actually, there is a lack of knowledge on the culture requirements of Marble goby for the successful raising of fry up to sub-adult size of 50 to 100g. The sub-adult size is considered an important stage to support Marble goby production because it is the size that is required for growing out in cage culture.

A stocking rate of 100-150 fish/m² of 50-100 g in individual weight is suitable for cage culture (Rakbankerd 2005). In this system, harvesting is performed periodically by size selection of between 400 and 1,200g.

Marble goby of average size of 81 g can live well in water with 4.5-7.8 ppm dissolved oxygen, a PH of 6.6 –7.3 and temperature between 27 and 31.4°C (Vu Cam Luong et al 2005). However, there is no information published on the tolerance limits and physiological responses of Marble goby according to changes in water quality.

Tra catfish (Pangasius hypophthalmus)

Tra catfish (Pangasius hypophthalmus) is one of 28 species in the family Pangasiidae, of which the majority is in the genera Pangasius. Pangasiidae species are found primarily in the Mekong Delta, Viet Nam. This species also occurs in Cambodia, Laos, and Thailand (http://www.fishbase.org/) (Roberts and Vidthayanon 1991). The Mekong delta in the southern part of Vietnam is known as the region for catfish farming, where Pangasianodon hypophthalmus has been traditionally farmed in small ponds using wild seed.  Commercial culture in cages, pens, and ponds commenced with the development of artificial mass seed production in 2000 (Nguyen Anh Tuan et al 2003). This fish is very popular and has served as a daily food for many Vietnamese people who live in the southern part of Vietnam, especially in the Mekong Delta.

Tra catfish has a long body, latterly flattened with no scales, a relatively small head, and broad mouth with small sharp teeth on the jaw and palatal bones. It has relatively large eyes and two pairs of barbels, the upper shorter than the lower. The fins have a dark grey or black color and six branched rays on the dorsal fin. Gill rakers develop normally and small gill rakers are regularly interspersed with larger ones. The fingerlings have a black stripe along the lateral line and another long black stripe below the lateral line. Large adults are uniformly grey but sometimes with greenish tint and silvery sides (FAO 2010).

Tra catfish (Pangasius hypophthalmus) is a migratory species. The fish moves upstream of the Mekong River at the end of the flooding season (from October to February) for spawning and the young fish return to the main stream at the beginning of the rainy season (from June to August). Khone Falls on the Lao-Cambodia border is known as the spawning ground of Tra catfish (MRC 2002, cited by Trinh Quoc Trong et al 2002). The young fish drift downstream with the water current and are swept into flooded areas in the southern part of Cambodia and the Mekong delta in Vietnam. Tra catfish is omnivorous, feeding on algae, higher plants, zooplankton, and insects, while larger specimens also take fruit, crustaceans and fish. Mature fish peak at a total length of 130 cm and up to 44 kg in weight. This species is typically living within the ranges of pH 6.5-7.5 and temperature 22-26 °C. Females take at least three years to reach sexual maturity in captivity when the weight is over 3 kg. However, males often mature in their second year but probably take about the same time as females in the natural habitat. Natural brood stock typically spawn twice annually but in cages in Viet Nam have been recorded as spawning a second time 6 to 17 weeks after the first spawning (FAO 2010).

 Pangasianodon hypophthalmus is a species which can be air-breathing (Browman and Kramer 1985 cited by Cacot 1999). Thus, this fish can live at low levels of dissolved oxygen. However, it prefers deep and flowing water, and therefore, farming areas of Tra catfish are mostly along the branches of the Mekong River and large canals.

The feed for Tra catfish in the 1990’s was farm-made, prepared from various ingredients such as trash fish, rice bran, soybean meal, blood meal, broken rice, cottonseed flour, milk, eggs and vegetables, supplemented with Vitamin C and E premixes. The ingredients were mixed together, cooked and fed in balls or extruded into noodle strands or pellets. However, with food safety concerns and fluctuating farm-made feed quality, there is an increasing trend towards the use of commercial pellets from 2008. The unit cost of farm-made feeds is cheaper but these feeds have feed conversion rate about 2.8-3.0 and cause greater water quality deterioration. In Viet Nam, larger-scale producers only use commercial pellets, while medium-scale producers usually used farm-made feeds for raising table tra catfish (FAO 2010).

Livestock manures and plants for earthworm cultivation

Animal manure composition

Animal manure is abundant in the countryside and frequently a source of environmental pollution in intensive animal agriculture. By contrast, the efficient recycling of this resource in an integrated farming system can lead to increased profit and decreased environmental damage (Preston 1996). Manure is rich in nutrients (Table 1) and is especially suitable for cultivating earthworms.

There are many reports on the effects of various animal wastes on growth and reproduction of earthworms. According to Chaudhuri and Gautam Bhattacharjee (2002), biomass production and reproduction of the earthworm Perionyx excavatus in four experiments with cow dung alone and in mixtures with straw, bamboo leaf litter or kitchen waste, showed maximum rate of biomass increase and reproduction in the mixtures with straw and bamboo leaf litter. Edwards et al (1998) reported that P. excavatus grew at similar rates in cattle manure, pig manure and aerobically digested sewage sludge, but the earthworms did not grow well in horse manure and grew only poorly in turkey excreta. However, the rate of growth and the time of maturation of this species were different under various population densities and temperatures between 15 and 30⁰C. The highest rates of reproduction occurred at 25 ⁰C both in cattle manure and sewage sludge. The species of earthworm also affects biomass production, fecundity and maturation. Surindra Suthar (2009) reported that the mean individual biomass of P. sansibaricus (768 mg) was higher than for P. excavatus (613 mg).

Water hyacinth

Water hyacinth (Eichhornia crassipes) is a fast growing perennial aquatic plant found in wetlands and which prefers nutrient-enriched water (Wilson et al 2005). It can cause infestations over large areas of water surfaces and leads to series of problems such as decrease of biodiversity, blockage of rivers and drainage systems, depletion of dissolved oxygen, alterations in water chemistry, environmental pollution, decreased fish population, restricting access to fishing sites and loss of fishing equipment – all of which result in reductions in catch and subsequent loss of livelihoods (Malik 2007). Therefore, many ways have been developed using biological, chemical and mechanical methods for preventing the spread and even eradicating water hyacinth. On the other hand, much attention has been concentrated on the potential of using water hyacinth for a variety of applications (see the review of Gunnarsson and Petersen 2007). For example, production of handicrafts, paper, ropes and furniture have been reported. According to Gunnarsson and Petersen (2007), water hyacinths are rich in nitrogen, (up to 3.2% of DM) and have a C/N ratio around 15. Thus, water hyacinth was proposed as a substrate for compost or biogas production. The sludge from the biogas process contains almost all of the nutrients of the substrate and can be used as a fertilizer for plants. Water hyacinth compost used as fertilizer on different crops has resulted in improved production.

The high protein content makes the water hyacinth a potential feed for livestock such as cows, goats, sheep and chickens. Abdelhamid and Gabr (1991) after chemical analysis on water hyacinths collected from a canal and a ditch reported them as having 9.5% DM, and in the DM 74.3% organic matter 19% crude protein and 18.9% crude fiber. Poddar et al (1991) reported the chemical composition of water hyacinth as 83.6% organic matter, 16.3% crude protein and 16.4% crude fiber (on DM basis) (cited by Gunnarsson and Petersen 2007). Aboud et al (2005) reported that water hyacinth could provide large quantities of nutritious feed and was a potential source for ruminant nutrition. In addition, it was recently realized that water hyacinth could be a potential biofuel crop and used in biofuel production (Bhattacharya and Kumar 2010). According to Gajalakshmi et al (2001), water hyacinth could be converted to compost by earthworms.

Water quality in ponds

Temperature

Rowland (1986) indicated that many fish species appropriate for aquaculture will survive and reproduce over a wide temperature range, but the temperature for maximum growth is narrower. For instance, a species can tolerate temperatures of 5 to 36⁰C but the range for maximum growth could be from 25⁰C to 30 ⁰C. However, the fish species in tropical and subtropical latitudes will not growth well when the temperature of the water is lower than 26 - 28 ⁰C. The temperature in our experiment varied from 28.1 to 29.5⁰C and thus was appropriate for normal growth of marble goby and Tra catfish.

Dissolved oxygen (DO)

The oxygen requirement of aquatic animals is quite variable and depends on the species, food intake, activity, size, water temperature and the dissolved oxygen concentration. Dissolved oxygen is probably the most critical water quality variable in freshwater aquaculture ponds. Dissolved oxygen concentrations are different between day and night time. Dissolved oxygen in the water is obtained through diffusion from air into water by mechanical aeration such as wind or aeration systems and biological transformation such as photosynthesis by aquatic plants.

According to Swingle (1969), warm water pond fish would die in a short time if dissolved oxygen fell to less than 0.3 mg/liter. A range from 0.3 to 1.0 mg/liter of dissolved oxygen concentration is lethal for fish if exposure is prolonged.  The fish survive but growth will be slow from prolonged exposure to dissolved oxygen concentrations from 1.0 to 5.0 mg/liter. More than 5.0 mg/liter of dissolved oxygen is desirable for almost all fish species in warm water ponds.

Andrews and Matsuda (1975) showed that the oxygen consumption rates of Channel Catfish one hour after feeding were higher than those taken immediately after feeding or from fasted fish.

pH

The relationship of pH of pond waters to their suitability for fish culture was discussed by Swingle (1961). The acid and alkaline death points are approximately pH 4 and pH 11, respectively. However, the optimum range for fish production is from pH 6.5 to pH 9. A pH range from 4 to 6.5 will result in the fish having a slow growth rate. 

In our research (Paper II), the pH did not change so much, and ranged from 7.05 to 7.34 in the morning and from 7.12 to 7.28 in the afternoon. These values are within the desirable range for fish growth and reproduction.

Nitrogen and the nitrification process

Nitrogen in the fish pond comes from waste products such as feed residues and fish excreta. These can be converted into nitrate (NO₃^-), which is non-toxic for fish.  This chemical reaction for the nitrification process is:

                                                                      Nitrosomonas

2 NH₃     +   3.5 O₂   ----------------->   2NO₂^-   +   2H₂O

                                (Ammonia) (Oxygen)                            (Nitrite)    (Water)

                                                                        Nitrobacter

                                  2NO₂^-   + O₂   ----------------->    2NO₃^-

                                          (Nitrite) (Oxygen)                     (Nitrate)

In this process, nitrite is an intermediate fish waste compound that is formed when ammonia is transformed to nitrite by Nitrosomonas bacteria activity. This particular group of bacteria uses ammonia as their food source, producing a waste product “nitrite”. Other groups of bacteria use nitrite as a food resource and produce nitrate as waste. Nitrate is a compound that is not toxic to fish at concentrations typically found in ponds. Another way to reduce ammonia in the water pond is for it to be used directly by phytoplankton (aquatic plants).

Total ammonia nitrogen (TAN)

Total ammonia nitrogen (TAN) is the combination of two forms of ammonia: NH₃^- and NH₄⁺. The NH₃^- form is toxic to fish at low levels, while NH₄⁺ is relatively non-toxic. Both forms of ammonia are present in fish culture systems. However, the amounts are dependent on temperature and pH. Water pH has the most influence on the direction in which the equilibrium equation will shift:  NH₃ + H₂O = NH₄OH = NH₄⁺ + OH^-. The reaction will shift to the right when the pH value is low; when pH is increased the reaction will shift to the left.

Toxic concentrations of NH₃-N for many pond fish in short-term exposure vary between 0.6 and 2 mg/litre, and some effects can be seen at 0.1 to 0.3 mg/litre (Boyd 1979). The safe levels of ammonia concentrations, recommended for long-term exposure, are below 0.05 mg/litre as NH₃-N and 1.0 mg/litre as TAN. In our study mean total ammonia nitrogen concentrations were low (from 0.158 to 0.206 mg/liter) thus they should not have affected fish growth.

Nitrite

Nitrite (NO₂^-) is toxic for fish when it is absorbed by fish and reacts with hemoglobin to form methemoglobin (Met-Hb). In this reaction, the iron in the “hem” of hemoglobin is oxidized from ferrous to ferric state, so it can not combine with oxygen to bring this compound to the essential organs of the fish. For that reason, reducing activity of hemoglobin or anemia is called nitrite toxicity or metheglobinemia. The blood of fish that contains significant amounts of methehemoglobin is brown in colour, so the common term for this poison is “brown blood disease”.

According to Greeley (1998), nitrite levels should not exceed 0.10 mg/1iter in pond water for channel catfish or 0.50 mg/1iter for salmonids. However, nitrite levels typically range from 0.5 to 5 mg/litre in fish ponds, probably due to the reduction of nitrate in anaerobic mud or water (Boyd 1982). High ammonia levels can be treated by adding chloride salt (in the form of sodium chloride or calcium chloride) to the water. The level of salt needed is less than 50 mg/liter which is not toxic to freshwater fish.

Protein and amino acid requirements of fresh water fish

According to NRC (1993) the protein and amino acid requirement do not differ greatly among fish species. However, the exceptions can often be identified with warm-water or cold-water, finfish or crustacean, omnivorous or carnivorous, and freshwater or marine fish. Therefore, nutrient requirements of these species are not available that can be chose prudence as the nutrient requirement of the other analogy species to using for these species.

Protein in the diets is a component decides the price of feed. The feed rice is high when the feed have high protein. The nutrient requirement of some fish species on juvenile stage was presented by some authors (Table 2)

Although, the protein quantity much more contributed on the growth rate of fish but the protein quality  also very important effect on their performance which showed by amino acid content. For optimal utilization of dietary protein, the amino acid content of the feed should closely resemble these essential amino acid requirements of the fish.

Earthworms as a feed source for livestock and fish production

Biology of earthworms

Perionyx excavatus is an earthworm with an iridescent blue or violet sheen on its skin which can be seen clearly under bright light. It is a very small worm so is suitable to use as fishing bait. This species has an impressive growth and reproductive rate, far in excess of the other species grown in bin culture (Darwin (1881) cited by Saheme bin Hashim (2008).

According to Sherman (2003), the different species of earthworms have similar physical structure. Earthworms belong to the phylum Annelida. They have many segments in their body, and they move by extension and retraction of these segments. The digestive tract of the earthworm extends the whole length of its body. They breath though their skin and can live in the water for a long time. They die if their skin becomes dry. Earthworms have both male and female sexual organs in their body. They have to find a partner for mating. The sperm is exchanged between two bodies when mating and stored in one of the segments of the worm. The cocoon casing is produced in mature worms. The cocoon is 2 to 4 mm in diameter. The time for cocoons to become the young worn is several months, depending on worm species and the immediate environmental. Earthworms can only reproduce using sperm from members of their own species.

Roles of earthworms in waste recycling

Earthworms have been projected as the major organisms to convert organic waste resources into value-added products, i.e., vermicompost and worm biomass. A wide range of organic wastes have been studies as feed material for different species of earthworms: for example,  water hyacinth (Gajalakshmi et al 2001), sewage sludge (Benite et al 1999), kitchen waste (Chaudhuri et at 2000), crop residues (Sudha Bansal and Kapoor 2000), cattle manure (Allan Mitchell 1997), neem leaves (Gajalakshmi and Abbasi  2004), straw, bamboo leaf (Chaudhuri and Gautam Bhattacharjee (2002), solid textile mill sludge (Priya Kaushik and Garg 2003), goat manure (Loh et al 2005), manure from sheep, donkey, buffalo, goat, cow, horse, camel (Garg et al 2005), activated sewage sludge (Ndegwa and Thompson 2001), turkey wastes (Edwards et at 1998), fresh leaves of mucuna and cacahuatillo, litter of macadamia and sawdust (García and Fragoso 2003), pig waste (Nguyen Hieu Phuong 2008) and duckweed (Kostecka and Kaniuczak 2008).   

Nutritive value of earthworms

Earthworms have high nutrient value, as described in many studies (Table 3).

Earthworms as a protein source for livestock and fish production

A study to evaluate the influence of feed supplemented with worms on the growth and meat quality of broiler chickens indicated that the diets with 2% worms supported the highest live weight at 10 weeks and the highest percentage of breast and leg meat (Vu Dinh Ton et al 2009).

The utilization of earthworm meal as a protein source in aquaculture feeds is poorly studied. Tuan and Focken (2009) reported that fish fed diets contained 30%, 70% and 100% of fish meal protein, replaced by earthworm meal had similar or higher growth rate, protein efficiency, and energy retention than those fed the fish meal based control diet. In the study conducted by Yaqub (1997), the growth performance and feed conversion ratio of catfish (Heterobranchus isopterus) fry over 30 days was better on earthworm meal than on fish meal.

Evaluation of earthworm (Hyperiodrilus euryaulos) meal as protein source in diets for Heterobranchus longifilis fingerlings under laboratory condition (Sogbesan and Madu 2008) revealed that 25% replacement of fish meal by earthworm meal supported higher net gain in weight and specific growth rate than fish fed 0 (control), 50, 75 or 100% earthworm meal. 

According to Pereira and Games (1995), in a study on growth of rainbow trout (average weight1500g), those fed a diet supplemented with frozen earthworms (Eisenia foetida) had decreased lipid in the carcass compared with fish fed diets containing 25, 50 and 75% frozen earthworms. Stafford and Tacon (1984) showed that earthworms of the species Dendrodrilus subrubicundu, collected from the trickling filter beds of a domestic sewage works and freeze dried, could replace 10, 50 and 100% protein meal in the diets of rainbow trout. There was no loss in fish performance at low levels of dietary inclusion (10% protein replacement) but a decline in fish performance at higher levels (50 and 100% protein replacement).

The experiment reported in Paper II also showed decreased growth rate of Marble goby and Tra catfish when frozen earthworms replaced a mixture trash fish, rice field prawn and rice bran.

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