DHA enrichment of the red earthworm Eisenia fetida for improving its potential as dietary source for aquaculture
Introduction
In aquaculture, fishmeal and fish oil are considered to be crucial dietary sources of proteins and lipids, respectively, to efficiently meet the essential amino acid and fatty acid requirements for cultured fish and crustaceans (Medale and Kaushik, 2009; Turchini et al., 2009; Jobling, 2016). When it comes to dietary lipids, it is well known that farmed marine animals, as with all vertebrates, cannot de novo synthesize polyunsaturated fatty acids (PUFA). It is also known that if PUFA are provided in their diets in the form of C18 PUFA (PUFA with 18 atoms of carbon, such as those found in terrestrial vegetable oils) most of the farmed marine animals cannot, or have very limited capacity to, bioconvert them into long chain PUFA (LC-PUFA), such as EPA (eicosapentaenoic acid; 20:5n-3) and DHA (docosahexaenoic acid; 22:6n-3) (Castro et al., 2016). Therefore, for cultured marine species, n-3 LC-PUFA are considered to be essential nutrients, as they are very important for various physiological processes, and therefore must be present in dietary meaningful quantities (Turchini et al., 2009; Tocher, 2010). However, n-3 LC-PUFA containing raw materials available for the aquaculture feed (aquafeed) industry are currently limited to marine derived products such as fish oils, which are restricted in their supply, under increasing demand and thus resulting in constantly increasing prices (Turchini, 2013). Reducing production costs, improving overall system efficiency and increasing environmental sustainability have always been priorities in the aquaculture and aquafeed sector. Thus, the search for alternative protein and lipid sources, to substitute and/or reduce the dependence upon marine resources, has been one of the main targets of the aquaculture sector since its global expansion 50 or so years ago (Jobling, 2016).
In this context, earthworms, though increasingly cultivated for vermicompost production in many countries, may well be considered to be an underutilised, and yet understudied, but potentially promising resource. These invertebrate animals can be efficiently cultured in great quantities, at cheap production costs and with very simple technologies. They are reared on decaying/fermenting organic matters of almost any kind, such as cow, sheep, goat, poultry, pig and horse manures, as well as all type of plant and animal matters, food and feed wastes and various agricultural by-products (Chauhan et al., 2010; Fairchild et al., 2017). Among many species, the red Californian earthworm (Eisenia fetida) is the most suitable for captive production and currently the most commonly farmed species worldwide. Earthworms have been reported be rich in protein, essential amino acids, n-3 PUFA as well as a suite of minerals and trace elements (Stafford and Tacon, 1985; Paoletti et al., 2003; Istiqomah et al., 2009). The quality and quantity of amino acid contents of earthworms have been reported to be comparable to that of fish meal (Tacon et al., 1983; Tacon and Metian, 2009; NRC (National Research Council), 2011), but their amino acid composition has also been reported to be variable from one species to another and relative to the food type they have been feeding upon (Tacon et al., 1983; Dong et al., 2010).
Earthworms (E. fetida) have been reported to be a good source of n-3 PUFA and EPA in particular, but limited in their DHA content (Liu et al., 2008; Beksari, 2017). Thus, earthworms' DHA content has been suggested to require attention before their possible use in feed for marine cultured species, particularly if to be used as broodstock feed (Liu, 2006). Darmawiyanti (2013) has been the first researcher to report that an earthworm species (Pheretima sp.) could be enriched in their nutritional composition. Specifically, in that study, it was reported that phospholipid, cholesterol and beta-carotene content of the earthworm can be improved, and that the enriched-worms could be successfully used as feed for shrimp (P. vannamei) broodstock, instead of marine worms (Nereis sp.). To the best of authors' knowledge, so far there has been no attempt to study the possible enrichment of the earthworm E. fetida for n-3 LC-PUFA, and especially for DHA. If DHA enrichment is proven doable, earthworms could have good potentials to be utilized as live, fresh or in dried forms, instead of more expensive marine counterparts, particularity for broodstock in marine hatcheries.
The aim of this study was therefore to evaluate the potential effects of an enrichment solution on the n-3 LC-PUFA, and especially DHA, content in the earthworm E. fetida. To achieve this, the response to the enrichment solution was tested at different, graded doses (0–50%), for different periods of time (0–96 h), and with or without the presence of bedding material, in two different experiments. Ultimately, the objective of this study was that of assessing the potential DHA fortification of earthworms, to provide the basis for their possible utilisation in marine hatcheries, as well as for other uses in the aquafeed industry.
Section snippets
General culture conditions
This study was carried out in the Mariculture R & D Centre of the Faculty of Fisheries of Çukurova University, Adana - Turkey. The red earthworms (Eisenia fetida) specimens used for the in vivo experiments were obtained from a commercial producer (Argesol Tarım Hayvancılık San. Tic. Ltd., Balıkesir - Turkey). After transport, earthworms were cultured using standard procedures in three plastic tanks (0.6 × 3 × 0.5 m) for several weeks before being used in the experiments. The compost material
Results
The fatty acid results showed that the non-enriched earthworms used in this study contained 20.16–22.00 mol% SFA, 25.95–26.90 mol% MUFA and 51.08–53.00 mol% PUFA (Table 1, Table 2, Table 3). In the initial and control (non-enriched) earthworms, the levels of some of the main PUFA, for example 18:2n-6 (10.30–11.35 mol%), 18:3n-3 (10.17–12.22 mol%) and eicosapentaenoic acid, EPA, 20:5n-3 (8.44–11.02 mol%), were relatively high, whereas in contrast, docosahexaenoic acid, DHA, 22:6n-3, was found to
Discussion
The present study demonstrated that: i) although the red earthworm E. fetida contains relatively high levels of PUFA, their natural DHA content is very limited, as previously observed by Liu et al. (2008) and Beksari (2017); but ii) the DHA content of the earthworm can be dramatically improved by specific dietary enrichment, and this, to the best of authors' knowledge, is the first report of such potential. The objective of this study was indeed to assess if earthworms nutritional composition
Conclusions
This study has demonstrated that n-3 PUFA and specifically DHA content of the red earthworm E. fetida can be elevated to levels up to 8–9 folds over the control worms by simply adding a commercial enrichment solution into their culturing compost. In order to effectively boost DHA level of the worms, a 12 h short enrichment period can be recommended when the bed-free enrichment technique is used, while longer periods of preferably 96 h should be chosen if the bedding technique is preferred. For
Acknowledgment
This study was supported by the Scientific Research Fund of Cukurova University (Grant No: FDK-2016-6272).
References (43)
- et al.
Review: long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of fads and Elovl gene repertoire
Prog. Lipid Res.
(2016) - et al.
The effect of egg fatty acid concentrations on embryo viability in wild and domesticated walleye (Stizostedion vitreum)
Aquat. Living Resour.
(1998) - et al.
Production and nutritional composition of white worms Enchytraeus albidus fed different low-cost feeds
Aquaculture
(2017) - et al.
A simple method for the isolation and purification of total lipids from animal tissues
J. Biol. Chem.
(1957) - et al.
Methods for assessing the composition and diversity of soil microbial communities
Appl. Soil Ecol.
(2000) - et al.
Use of the brine shrimp, Artemia spp., in marine fish larviculture
Aquaculture
(2001) - et al.
A preliminary investigation of the nutritive value of three terrestrial lumbricid worms for rainbow trout
Aquaculture
(1983) - et al.
Responses of striped bass larvae fed brine shrimp from different sources containing different fatty acid compositions
Aquaculture
(1990) - et al.
The effect of earthworm (Eisenia fetida) and vermihumus meal in diet on broilers chicken efficiency and carcass components
Biol. Forum
(2015) Enrichment of HUFA Contents of the Earthworm Eisenia fetida and It's Use as Feed for the Shrimp Penaeus vannamei
(2017)
Vermicomposting of vegetable wastes with cowdung using three earthworm species Eisenia foetida, Eudrilus eugeniae and Perionyx excavatus
Nat. Sci.
Using a fermented mixture of soybean meal and earthworm meal to replace fishmeal in the diet of white shrimp, Penaeus vannamei (Boone)
Aquac. Res.
The Evaluation of Earthworm (Pheretima Sp) Enrichment on the Chemical Composition and Ovarian Development of Female Pacific White Shrimp (Litopenaeus vannamei) Broodstock
Apparent digestibility of selected feed ingredients in diets for juvenile hybrid tilapia, Oreochromis niloticus × Oreochromis aureus
Aquac. Res.
Effect of dried earth worm (Aporrectodea caliginosa) as replacement of fish meal on growth and survival rate of the freshwater prawn, Macrobrachioum rosenbergii (DE MAN 1879) larvae
Egypt. J. Aquat. Biol. Fish.
Profile of amino acids, fatty acids, proximate composition and growth performance of Tubifex tubifex culture with different animal wastes and probiotic bacteria
AACL Bioflux
Enrichment of the nematode Panagrolaimus sp., a potential live food for marine aquaculture, with essential n-3 fatty acids
Aquac. Int.
Amino acids profile of earthworm and earthworm meal (Lumbricus rubellus) for animal feedstuff
J. Indones. Trop. Anim. Agric.
Fish nutrition: past, present and future
Aquac. Int.
Larval pigmentation, survival and growth of Penaeus indicus fed the nematode Panagrellus redivivus enriched with astaxanthin and various lipids
Aquac. Nutr.
Replacement of fishmeal with locally available ingredients in diet composition of Macrbrachium dayanum
Afr. J. Agric. Res.
Cited by (7)
Functionally diverse front-end desaturases are widespread in the phylum Annelida
2023, Biochimica et Biophysica Acta - Molecular and Cell Biology of LipidsValorisation of industrial food waste into sustainable aquaculture feeds
2023, Future FoodsFeed Ingredients for Sustainable Aquaculture
2023, Sustainable Food Science - A Comprehensive Approach: Volumes 1-4Natural Biota's Contribution to Cultured Aquatic Animals' Growth in Aquaculture Cannot Be Ignored
2023, Aquaculture ResearchTerrestrial Sources of Polyunsaturated Fatty Acids for Aquaculture
2021, Journal of IchthyologyN-3 lc-pufa enrichment protocol for red earthworm, eisenia fetida: A cheap and sustainable method
2021, Turkish Journal of Fisheries and Aquatic Sciences