Abstract
Sustainable food system innovations are urgently needed to feed a growing human population while staying within planetary boundaries. Farmed edible insects have received considerable scientific and public attention due to their potential to improve food system circularity by upcycling nutrients from organic residual streams to nutritious food. Earthworms, as non-insect invertebrates, have remained largely unrecognized in the future foods debate. However, they are already widely farmed at industrial scale for their capacity to recycle organic wastes and improve soil fertility. We conducted a systematic literature review to provide a quantitative basis on earthworm nutritional composition, thereby positioning earthworms in the future foods debate. Here we show, based on evidence from 142 scientific studies, that farmed earthworms are a potentially interesting food source. They have an attractive nutrient composition compared to the main farmed edible insect species, being especially rich in protein, low in fat and containing a favourable profile of essential amino acids. The content of important fatty acids, minerals and vitamins in earthworm biomass is higher or lower than in edible insects, depending on the feed material. Crude protein and fat contents are higher in farmed versus wild earthworms, indicating that farming conditions provide a lever for further improving the nutritional composition of earthworm biomass. Whether earthworm species or feed materials affect earthworm nutritional composition could not be finally clarified based on the available data. We conclude that earthworms have high potential as a future food from a nutritional perspective, mainly as an alternative source of protein. The integration of earthworm farming in future food systems can be expected to improve sustainability and circularity, potentially giving earthworms an advantage over edible insects.
1 Introduction
The global population and thereby the demand for food continue to grow (United Nations, 2022), while current food production systems are increasingly jeopardized by environmental degradation (Mirzabaev et al., 2023). Food production, especially animal husbandry, is also a major driver of environmental degradation and greenhouse gas emissions (Pelletier and Tyedmers, 2010). Future food systems will therefore need to combine a reduction of environmental impact with increased resilience to weather extremes and sufficient production of healthy food (Willett et al., 2019; Herrero et al., 2020). Future foods, such as edible insects, algae, or fungi, have been proposed as nutritious and sustainable alternatives to conventional animal-derived foods that have a high environmental impact (Grimm and Wösten, 2018; Parodi et al., 2018; Ullmann and Grimm, 2021). Future foods are defined as scalable technologies that facilitate high productivity within controlled conditions, require minimal space, and consequently hold potential to reduce land-use and greenhouse gas emissions (Parodi et al., 2018; Mazac et al., 2022).
Besides being environmentally sustainable, future foods also need to provide sufficient nutrients for a healthy diet. The nutritional quality of future foods, as of any other food, can be evaluated based on their proximate composition, which includes moisture, ash, lipid, protein and fibre contents (Thangaraj, 2016). Nutritional quality is further defined by the content of specific organic compounds, such as amino and fatty acids. Amino acids are the building blocks of protein (Hambræus, 2014). The essential amino acids are of special importance, as they cannot be synthesized by the human body and need to be taken up with food (World Health Organization, 2007). The same applies to the essential unsaturated fatty acids cis-linoleic acid (LA, 18:2) and α-linolenic acid (ALA, 18:3) (Das, 2006). Their metabolic successors arachidonic acid (ARA, 20:4), eicosapentaenoic acid (EPA, 20:5) and docosahexaenoic acid (DHA, 22:6) can be synthesized in the human body, but are also an important component of healthy diets (Kaur et al., 2014). Further important nutrients are minerals and vitamins, where deficiencies are common in calcium, iodine, iron and zinc and the vitamins A, folic acid and cobalamin (B12) (Sanghvi et al., 2007; Harinarayan et al., 2021).
Insect farming has received considerable scientific and public attention in the future foods debate but important drawbacks have remained unattended. Insects are rich in protein and contain a complete fatty acid profile (Finke, 2002). In the European Union four species are currently approved for commercialisation as food under the Novel Foods Legislation (Regulation (EU) 2015/2283, 2015), and others are under evaluation. Commonly farmed insects, such as black soldier fly larvae (Hermetia illucens, Linnaeus 1758), house crickets (Acheta domesticus, Linnaeus 1758), and yellow mealworms (Tenbrio molitor, Linnaeus 1758) can be fully or partially fed with organic residual streams, and hence allow upcycling of nutrients to protein-rich food or feed (van Huis, 2020). However, current practice in insect farming often deviates from this ideal due to EU Regulations, which limit the range of approved feed materials (Żuk-Gołaszewska et al., 2022). As a result, high quality feeds such as cereal flour, soymeal, skimmed milk and compounded chicken feed (Makkar et al., 2014; Dobermann et al., 2017; Bosch et al., 2020; Oonincx et al., 2020) are commonly used in insect farming. This practice calls for a feed-versus-food debate and raises questions on environmental sustainability (Gianotten et al., 2020; Parodi et al., 2022). In addition, insect farming requires precisely controlled environmental conditions, including lighting, ventilation and particularly temperature regulation (Cortes Ortiz et al., 2016). The associated energy costs of insect farms currently pose a limitation to scalability in temperate regions (Halloran et al., 2016; van Huis and Oonincx, 2017). For these reasons it is interesting to also look at other invertebrates, the potential of which has so far been under-explored. In particular, less heat dependent, detrivorous invertebrates such as earthworms are potential candidates as future foods.
Earthworm farming, also referred to as vermiculture, is practiced at industrial scale since the late 1970s (Edwards et al., 2011). The potential of using earthworm biomass as a protein source for human nutrition (Sun and Jiang, 2017), however, remains currently unrealized. Earthworms play a key role in nutrient cycling and soil fertility (Blouin et al., 2013). In vermiculture, this capacity is utilized to recycle organic wastes and produce vermicompost, a high-quality organic fertilizer (Rehman et al., 2023). Optimal culture conditions for earthworms are well established (Edwards and Dominguez, 2011; Lowe et al., 2023) and employed worldwide in vermiculture systems ranging from low-tech to industrial scale (Sherman, 2018). These systems are generally based on litter-dwelling (epigeic) earthworms (Lowe et al., 2023), which consume decomposing organic materials, as opposed to endogeic and anecic earthworms, which live in and primarily consume mineral soil with associated decomposed organic matter (Bouché, 1977). Five litter-dwelling species are preferred in vermiculture due to their high reproductive rates and adaptability to variable culture conditions (Edwards and Dominguez, 2011). This includes the temperate species Eisenia andrei (Bouche, 1972), Eisenia fetida (Savigny, 1826), and Dendrobaena veneta (Rosa, 1886), and the tropical species Eudrilus eugeniae (Kinberg, 1866), and Perionyx excavatus (Perrier, 1872). The biomass of farmed earthworms can be used as a valuable protein source, as was first suggested by Lawrence and Millar in 1945. Earthworms are rich in protein and essential amino acids of comparable quality to other animal-based protein sources (Zhenjun et al., 1997; Sun and Jiang, 2017), and a good source of minerals and vitamins (Domı́nguez et al., 2017). Not surprisingly, earthworms are traditionally appreciated as food by diverse cultures around the world (Paoletti et al., 2003; Grdiša et al., 2013; Ding et al., 2019) and recognised as a suitable fish-meal replacement in poultry or aquaculture feeds (Parolini et al., 2020). While various authors have analysed the nutritional composition of earthworms and indicated their potential as human food (Sabine, 1983; Zhenjun et al., 1997; Sun and Jiang, 2017), a comprehensive overview is currently lacking and earthworms remain largely unrecognized in the ongoing debate on future foods.
The primary aim of this article is to establish a quantitative basis for the nutritional quality of earthworms, thereby positioning earthworms in the future foods debate. The research objectives were (1) to compare the nutritional composition of wild and farmed earthworms, highlighting potential effects of cultivation, (2) to investigate the effect of species and feed sources on earthworm nutritional composition, and (3) to compare the nutritional quality of earthworms with three species of commonly farmed edible insects. To this end, we conducted a structured literature review of scientific publications on earthworm nutritional characteristics.
2 Methodology
2.1 Literature search strategy
The present review was performed according to the PRISMA guidelines (Page et al., 2021) and followed a two-round search process (Figure 1). We first searched scientific databases for publications of earthworm nutritional data (Round 1), and then searched for further references in those articles (Round 2), which were eligible based on predefined screening criteria. The search terms used in the first step were pilot tested in advance to ensure high relevance of search results. We performed the final database search on 9th March 2023 in Scopus and Web of Science including titles, abstracts and keywords and using the following search phrase:
“earthworm” AND (“food” OR “feed”) AND (“chemical composition” OR “protein”)
Duplicates and one erratum were removed from the search results before screening.
2.2 Screening: inclusion and exclusion criteria
The results of the database search (Round 1) were screened by title and abstract and sought for retrieval if they appeared to provide earthworm nutritional data. Retrieved reports were then assessed by the first author for eligibility and included in the review if they met the following criteria: (1) published as an original research article, book chapter, government report, workshop or conference proceedings, (2) written in a language read by the authors (English, German, Spanish) or containing data in a readable table, (3) provides data on nutritional characteristics of earthworms, including proximate composition, essential amino acids, fatty acids, minerals, and vitamins, (4) review articles, if original source could not be obtained. The exclusion criteria were: (1) does not provide relevant earthworm nutritional data, (2) review articles using non-original data, (3) data identical to a previous publication, (4) newspaper articles and PowerPoint presentations, (5) data contained errors. Eligible studies and excluded reviews were then used for citation searching (Round 2). Studies identified in the second round were submitted to the same screening process.
PRISMA 2020 flow diagram showing the systematic two-step search process used to identify literature for the present review. In round one (left side), literature was identified via databases, and in round two (right side), literature was identified via citation searching.
Citation: Journal of Insects as Food and Feed 10, 5 (2024) ; 10.1163/23524588-20230163
2.3 Data extraction and standardization
The 142 articles accepted for review were listed in a table (Supplementary Table S1), including title, authors, journal and year of publication. One reviewer then extracted the available earthworm nutritional data with corresponding units, including proximate composition, essential amino acids, fatty acids, minerals, and vitamins, to the table. In addition, one reviewer extracted information regarding the earthworm species, feed material, gut voiding, drying method and analysed material (fresh earthworms/earthworm meal).
The nutritional data was then standardized by one of the reviewers to ensure comparability and double checked by another reviewer. Dry matter (DM) and water content of fresh earthworms were calculated to percentage of fresh matter (FM). Proximate composition, essential amino acids, minerals and vitamins were calculated to % DM, if the water content was given and excluded from the dataset otherwise. Where total nitrogen but not crude protein was given in an article, we used the conversion factor of 6.25 to calculated crude protein. In some cases, tables or data were poorly labelled. A recurring example was the use of the term dry weight where earthworm meal containing around 9% moisture was analysed. In such cases we corrected the unit to wet weight, based on comparison with data from other articles. This approach was chosen to maintain a sufficient number of datapoints for our review, assuming that the analysis was done correctly and only the data described poorly in the concerned studies. Fatty acids were kept as % total fatty acids, because crude fat and water content of the original sample were often omitted in the respective articles. Data was excluded from the analyses if standardization was not possible due to missing information (e.g. water content), or if part of the data was erroneous (e.g. proximate composition > 100%). Earthworm species names were updated using DriloBASE (Drilobase Project, 2013) where possible.
Boxplots show the proximate composition of farmed and wild earthworms in comparison with three species of commonly farmed edible insects, which are indicated as point-ranges. Dots outside of boxplots are outliers and points in the point-ranges indicate the mean. The dry matter content is given as percentage of fresh matter, and all other nutrients are given as percentage of total dry matter. Earthworm data was compiled by the authors from individual studies and data for edible insects taken from recent reviews (Gkinali et al., 2022, Lu et al., 2022, Ververis et al., 2022). The number of datapoints were as follows: house cricket: n = 25, 36, 31, 35, 16, respectively for each component in the order of the figure; black soldier fly larvae: n = 0, 6, 6, 6, 3; yellow mealworm: n = 0, 13, 11, 12, 8.
Citation: Journal of Insects as Food and Feed 10, 5 (2024) ; 10.1163/23524588-20230163
For reference, we added data for three species of commonly farmed edible insects to Figure 2 and Figure 5. These species are house crickets, black soldier fly larvae, and yellow mealworms. Means and ranges for proximate composition were taken from recent reviews (Gkinali et al., 2022), or calculated from data given in, or as supplementary to a review (Lu et al., 2022; Ververis et al., 2022). Insect fatty acid data in Table 1 were gathered from Paul et al. (2017), and Oonincx et al. (2020). Values for essential amino acids in Figure 5 were either taken from recent reviews (Hong et al., 2020; Lu et al., 2022), or, in the case of house cricket, calculated from two individual studies (Finke, 2002; Udomsil et al., 2019). Data for mineral and vitamin content for edible insects in Tables 2 and 3, respectively, were taken from individual studies (Pennino et al., 1991; Finke, 2002, 2007, 2013; Zielińska et al., 2015; Latunde-Dada et al., 2016; Shumo et al.; Chia et al., 2020; Sikora et al., 2023).
2.4 Search results
As Figure 1 shows, a total of 274 records was found in the data base search (Scopus: 211, Web of Science: 63), including 64 duplicates. After screening by title and abstract, 93 reports were retrieved for full-text review, of which 49 were excluded for the following reasons: no earthworm nutritional data was provided (n = 30), reviews of non-original data (n = 10), data identical to previously published article (n = 8), data contained errors (n = 1). In this first round, 42 publications were accepted for review. In round two, we excluded one retracted article, and those already found and in- or excluded in the previous search (Round 1), and then screened 5,692 records by title. Of these, 288 were sought for retrieval as potential sources of earthworm nutritional data. We gathered 217 reports via publishers, websites or libraries of which 115 were excluded for the following reasons: no earthworm nutritional data was provided (n = 75), review of non-original data (n = 13), data identical to previously published article (n = 8), language not spoken by the authors (n = 17), data contained errors (n = 2). Finally, 100 studies were accepted in round two, adding up to a total of 142 included studies.
Of the 142 included studies, 133 provided full or partial data on proximate composition, 60 analysed essential amino acids, 39 minerals, 24 fatty acids, and seven vitamins. We found data on a total of 25 distinct earthworm species and two two-species combinations.
3 Farmed vs wild earthworms
Figure 2 shows the proximate composition of 10 farmed and 16 wild earthworm species compared to three species of commonly farmed edible insects, which are included as a reference. Live earthworms contain on average 18% dry matter (DM), which is predominantly composed of protein, followed by ash, fat and fibre.
Boxplots show the proximate composition of the five most commonly farmed earthworm species Dendrobaena veneta, Eisenia andrei, textitEisenia fetida, Eudrilus eugeniae, and Perionix excavatus. Larger dots indicate outliers. In D. veneta less than three datapoints were available, which are shown as small dots without boxplot.
Citation: Journal of Insects as Food and Feed 10, 5 (2024) ; 10.1163/23524588-20230163
We observe notable differences between the nutritional composition of farmed and wild earthworms (Figure 2), which are likely linked to differences in habitat, feed material and post-harvest handling. Farmed earthworms have on average higher crude protein, fat and fibre contents, while their ash content is lower than in wild earthworms. Earthworms can be classified according to their habitat and diet preferences (Bouché, 1971). In our data-set, 83.3% of farmed earthworms are litter-dwellers, while this is only the case for 35.3% of the wild earthworms. Accordingly, the majority of the wild earthworms are soil-dwellers, which can be expected to have more mineral particles in their gut than litter-dwelling species. Furthermore, farmed earthworms are usually fed with energy- and nitrogen-rich organic materials including manure, fruit and vegetable waste, or kitchen waste (Sherman, 2018), while wild earthworms typically consume feed of lower quality. Hence, better nitrogen and energy availability in the feed and less energy expenditure may contribute to higher protein and fat contents observed in farmed earthworms. Similarly, this has been observed for fat contents in farmed compared to wild insects (Oonincx and Finke, 2021). We found no difference in essential amino acid composition between farmed and wild earthworms.
The high variability of crude ash content in farmed and wild earthworms and the prevalence of outliers in farmed earthworms, are likely artefacts of methodological inconsistency in post-harvest handling. Only one third (n = 47) of the analysed studies report treatment to void the earthworms’ gut prior to analysis, and for varying periods of time (0.5–48 h). As a result, high ash and fibre contents observable in some studies negatively distort overall earthworm protein and fat contents. In summary, the use of feed materials with low mineral content and consistent voiding of the gut after harvesting of earthworms provide levers for improving their nutritional composition.
4 Commonly farmed earthworm species
The nutritional composition of the five most commonly farmed earthworm species (Edwards and Dominguez, 2011) is shown in Figure 3. E. fetida is by far the most abundant species in our dataset (ntotal = 107, nfarmed = 88), reflecting its ubiquitous use in vermiculture. It is followed by E. eugeniae (ntotal = 15, nfarmed = 9) and P. excavatus (ntotal = 12, nfarmed = 9), while D. veneta and E. andrei are underrepresented in our dataset compared to their use in commercial vermiculture.
Boxplots show the proximate composition of Eisenia fetida farmed on the following feed materials: fruit and vegetable waste, kitchen waste, manure, and a mix of manure and organic waste. If less than three datapoints were available, they are indicated as small dots without boxplot. Larger dots indicate outliers.
Citation: Journal of Insects as Food and Feed 10, 5 (2024) ; 10.1163/23524588-20230163
From the available data, it appears that nutritional differences between commonly farmed earthworm species are small. However, it is difficult to disentangle the effects of species, feed material, and vermiculture conditions given the few available datapoints for most species. Direct comparisons of several earthworm species in controlled feeding experiments are rare in the literature. Nonetheless, the studies we found indicate that protein content may vary up to 14% between species farmed under the same conditions (Tacon et al., 1983; Reinecke et al., 1991b; Kumar et al., 2022). Further investigation of this topic may help to select particularly nutritious earthworm species for human consumption. Certain earthworm species may also be preferable to others in terms of flavour (Cayot et al., 2009).
5 Eisenia fetida – a versatile eater
The most extensively farmed earthworm species, E. fetida, demonstrates adaptability to a wide range of feed materials without compromising its average protein content (Figure 4). However, there is considerable variation of up to 20% DM within the feed categories, showing that certain feeds, probably containing more ash, reduce the protein content. The effect of diet may be more pronounced in other, less adaptable earthworm species. Studies investigating this topic are extremely rare and do not reach consistent conclusions. Garcı́a et al. (2009) found variations of crude protein content in Eisenia spp. of up to 7% DM, which is notable considering the small differences in the feed mixes used by the authors. While diet appears to have limited effects on the nutritional composition of E. fetida, it is known as a key factor for productivity in vermiculture (Edwards et al., 2011; Sherman, 2018). Further studies should investigate the feed preferences of commonly farmed earthworm species so that they can transform organic residual streams to edible protein most efficiently.
Content of essential and other important fatty acids in earthworms and three species of commonly farmed edible insects given as the percentage of total fatty acids
Citation: Journal of Insects as Food and Feed 10, 5 (2024) ; 10.1163/23524588-20230163
6 Higher in protein and lower in fat – earthworms vs edible insects
The crude protein content in farmed earthworms is at least as high and variable as in farmed edible insects (Figure 2), with average values of 62.3% DM and 63.9% DM for farmed earthworms and house crickets, respectively. It has to be noted that the protein content of insects has often been overestimated due to non-protein nitrogen present in the form of uric acid, β-alanine, and chitin exoskeletons (Janssen et al., 2017; Hopkins et al., 2021; Oonincx and Finke, 2021). Chitin content also varies across insect species and life stages (Oonincx and Finke, 2021) and the use of adjusted nitrogen-to-protein conversion factors (Kp) has been suggested accordingly (Janssen et al., 2017). In the present review, 45 out of 60 studies used as references for insect protein content in Figure 2 applied the conventional Kp of 6.25 and therefore likely overestimated insect protein content. When corrected Kp of 4.43, 5.41 and 5.09 are used for black solder fly larvae (Smets et al., 2021), yellow mealworm (Boulos et al., 2020), and house crickets (Ritvanen et al., 2020), respectively, the actual insect protein content is reduced by 11.2%, 6.9%, and 11.9%, respectively. After such corrections, it becomes clear that farmed earthworms exceed important farmed insects in mean protein content. In earthworms, chitin is present in the gizzard epithelium (Peters and Walldorf, 1986), which is only 10-50 μm thick in L. rubellus (Yaqub, 1997b) and therefore is negligible in this context.
Earthworm fat content, with an average value of 8.6% DM, is half the value or lower than in farmed edible insects. The fatty acid composition of farmed earthworms was analysed by 14 studies in our dataset and results are summarized in Table 1. The reported variation of individual fatty acids may be related to fatty acid content of feed materials (Dynes, 2003a), but also differs seasonally and by species (Petersen and Holmstrup, 2000b; Holmstrup et al., 2007). The essential LA, and important ARA and EPA are present in earthworms at approximately 0.7, 1.0 and 1.2% of total dry matter, respectively. The proportion of ALA in the total fatty acids of earthworms is higher than in black soldier fly larvae, house crickets and yellow mealworms, while the proportion of LA is comparable to black soldier fly larvae, and lower than in house crickets and yellow mealworms (Paul et al., 2017; Oonincx et al., 2020). Fat content and fatty acid composition in insects are strongly influenced by feed material but also depend on species, life stage and environmental factors (Oonincx et al., 2020; Oonincx and Finke, 2021). The influence of feed material on the fatty acid composition of earthworms requires further investigation. Essential and other important fatty acids in earthworms may provide additional nutritional benefits, yet earthworms should be viewed primarily as a source of protein with a low fat content.
The crude ash content in farmed earthworms, with a mean of 11.7% DM, is slightly higher than that in farmed edible insects, of which black soldier fly larvae have the highest content with 8.2% DM. A potential explanation is that, although not strictly necessary, soil is often added to the substrate in vermiculture containers, thus increasing the amount of mineral particles in the earthworm gut. In addition, these mineral particles were not consistently voided from the earthworm gut in several studies and thus included in the analysis.
The crude fibre content of earthworms, with a mean of 3.5% DM, appears to be slightly lower compared to edible insects, where the lowest value is found in house crickets with 7.3% DM. The fibre fraction of earthworms and insects is not well studied. Fibre in insects is known to contain proteins, sclerotised proteins, minerals and other substances bound to chitin (Finke, 2007; Oonincx and Finke, 2021).
7 The favourable amino acid profile of earthworms
Earthworm protein contains a complete profile of essential amino acids (EAA) similar to that of edible insects (Figure 5). The most abundant EAA in earthworms are leucine and lysine, with means of 5.11 and 4.15 g/100 g DM respectively, while cystine, tryptophan, methionine and histidine are present in limited amounts, with means of 0.78, 0.84, 1.17 and 1.78 g/100 g DM, respectively. When compared to whole egg, which has been used as a standard for a high-quality EAA composition (Layman and Rodriguez, 2009), it is notable that earthworms contain larger amounts of all EAA per 100 g dry matter (United States Department of Agriculture, 2019). The essential amino acids lysine, threonine, cysteine, methionine and tryptophan, which are commonly limiting in imbalanced human diets (Hambræus, 2014), are 3.8, 3.5, 1.5, 2.1 and 3.8 times higher, respectively in earthworms than in whole egg. Thus, we emphasize that earthworms hold significant potential for addressing amino acid deficiencies in imbalanced human diets.
Boxplots show the content of essential amino acids in earthworms in comparison with three species of commonly farmed edible insects, indicated as point-ranges. Larger dots indicate outliers. Earthworm data was compiled by the authors from individual studies, and data for black soldier fly larvae (n = 7, 7, 7, 7, 7, 7, 7, 7, 3, 7, respectively for each amino acid in the order of the figure) and yellow mealworm (n = 6, 10, 10, 10, 10, 9, 9, 10, 4, 10) was taken from recent reviews (Hong et al., 2020; Lu et al., 2022), while data for house cricket (n = 2) was averaged from two individual studies (Finke, 2002; Udomsil et al., 2019).
Citation: Journal of Insects as Food and Feed 10, 5 (2024) ; 10.1163/23524588-20230163
8 Minerals and vitamins in earthworms
Earthworms could also be an interesting source of minerals and vitamins (Domı́nguez et al., 2017). The mineral content of earthworms and three species of commonly farmed edible insects is shown in Table 2. The reported variation in earthworms is likely linked to the mineral content of different feed materials (Oonincx and Finke, 2021), although this effect may be more pronounced for some minerals (Garcı́a et al., 2009). Heavy metals, for instance, are known to be accumulated in earthworm body tissue to varying degrees depending on the species, metal and concentration in feed material (Ireland, 1979; Hartenstein et al., 1980b; Ma, 1982; Neuhauser et al., 1995; Dai et al., 2004; Li et al., 2010). Heavy metals of food safety concern, such as cadmium and lead, have in some cases been found to exceed permissible limits for human consumption in farmed earthworms (Graff, 1982; Hilton, 1983; Stafford, 1984; Flores and Alvira, 1987; Pereira and Gomes, 1995; Regulation (EU) 2023/915, 2023). The mineral content of edible insects, including heavy metals, is also affected by the composition of feed materials, species and stage of development (EFSA Scientific Committee, 2015; van der Fels-Klerx et al., 2018; Ojha et al., 2021; Oonincx and Finke, 2021). Here, we focus on the minerals calcium, iodine, iron and zinc, which are commonly deficient in human diets (Sanghvi et al., 2007; Harinarayan et al., 2021). The calcium content in earthworms is lower than in black soldier fly larvae (Dierenfeld and King, 2008; Finke, 2013; Chia et al., 2020), and higher than in house crickets and yellow mealworms (Finke, 2002; Zielińska et al., 2015; Latunde-Dada et al., 2016; Köhler et al., 2019; Sikora et al., 2023). Iodine and iron contents are both higher in earthworms compared to the three species of edible insects and zinc contents are sometimes comparable, but may also be higher or lower in edible insects (Finke, 2007; Finke, 2013; Zielińska et al., 2015; Köhler et al., 2019; Chia et al., 2020; Sikora et al., 2023). Overall, farmed earthworms may contribute important minerals to human nutrition, if they are sufficiently present in the organic residues used as feed material and heavy metal contamination is checked.
Mineral content of earthworms and three species of commonly farmed edible insects
Citation: Journal of Insects as Food and Feed 10, 5 (2024) ; 10.1163/23524588-20230163
Information on earthworm vitamin content is scarce in the literature. The available data from five studies is given in Table 3. Here we limit ourselves to the important vitamins A, folic acid and cobalamin (B12), which are commonly deficient in human diets (Sanghvi et al., 2007). Vitamin A can be present at higher or lower concentrations in earthworms compared to the three commonly farmed edible insects used for reference (Pennino et al., 1991; Finke, 2002, 2013; Shumo et al., 2019b). Folic acid is found at lower and cobalamin at higher concentrations in earthworms compared to edible insects (Finke, 2002, 2013). These findings show that earthworms may be an interesting source of vitamin A, cobalamin and other B-vitamins. Most insect species cannot synthesize B-vitamins de novo (Oonincx and Finke, 2021); Instead, they are absorbed from feed and the associated microbiome (Douglas, 2017; Oonincx and Finke, 2021). The common use of compound chicken feed, containing a vitamin mix, in insect rearing (Oonincx et al., 2020) could explain higher contents of some vitamins in edible insects. Although this has not yet been confirmed by studies, it is plausible that earthworms also acquire B-vitamins from feed and the associated microbiome. The availability of B-vitamins in earthworm feed materials may therefore become an important variable in the production of earthworms for human nutrition.
Vitamin content of earthworms and three species of commonly farmed edible insects
Citation: Journal of Insects as Food and Feed 10, 5 (2024) ; 10.1163/23524588-20230163
9 Earthworms in future food systems
The role of earthworms in future food systems aligns closely with that of farmed insects as they can efficiently upcycle organic residual streams into earthworm-protein for human consumption and produce vermicompost as a valuable organic fertilizer (Lowe et al., 2023). Earthworm farming has three potential advantages over insect farming related to (1) energy-use, (2) the use of feed, and (3) the occurrence of diseases. First, farming earthworms, given that they are well-adapted to soil temperatures, requires less heating than farming insects outside tropical regions. Temperate and tropical earthworms tolerate temperatures of 0-35 °C and 15-35 °C, respectively, and activity in both is greatest around 25 °C (Edwards and Dominguez, 2011), while crickets and black soldier fly larvae require 30 °C and 25-30 °C, respectively (Ayieko et al., 2015; Shumo et al., 2019a). Second, earthworm farming can be profitable using only organic residual streams as feed, due to the high prices achieved by vermicompost (Sherman, 2018). Industrial scale insect farming in the Global North, on the other hand, at present frequently uses high-quality feeds to optimize economic efficiency and comply with EU regulation (Makkar et al., 2014; Oonincx et al., 2015; Dobermann et al., 2017; Bosch et al., 2020; Oonincx et al., 2020), which calls for a food-versus-feed debate and may increase the overall environmental footprint of the food system (Gianotten et al., 2020; Parodi et al., 2022). The situation is different in the Global South, where fly species are being farmed fully on organic residue diets (Dzepe et al., 2021). Third, to our knowledge no diseases have occurred in earthworm farming even though it is practiced at industrial scale for several decades. In contrast, disease outbreaks are becoming more problematic with the scaling up of insect production (Maciel-Vergara et al., 2021).
One could argue that competition over residual streams by different upcycling pathways is likely to intensify as we move towards more circular food systems. In this line of reasoning, introducing earthworm farming would only add another competitor into this landscape. Our vision is that instead of highlighting competition between various upcycling pathways such as farming of earthworms, insects, fungi, bacteria or chemical processing, we should embrace the synergies that these technologies offer within an anthropogenic ecosystem of upcycling pathways. By combining the strengths of different organisms and processes according to the properties of a residual stream, we could achieve a higher value use in social, economic and environmental terms. To this end, earthworms could be combined with a number of other upcycling pathways. For example, a study found that rearing of black soldier fly larvae can be effectively coupled with subsequent vermiculture (Cappellozza et al., 2019). The authors showed that feeding insect excreta to earthworms led to added value in terms of compost quality and earthworm protein. Earthworms have also been successfully employed to decompose spent mushroom substrates, a residual stream from the production of edible mushrooms (Hřebečková et al., 2020; Purnawanto et al., 2020). Thereby, spent mushroom substrate, which can cause nutrient leaching if left untreated, can be upcycled into earthworm protein and vermicompost (Ruangjanda et al., 2022). A similar coupling of vermiculture can be imagined for organic residual streams from fermentation-farming of microalgae and bacteria, or digestate from bio-energy production.
10 The way forward
Embedding earthworms in the transition towards sustainable and circular food systems will require, among other things, overcoming bottlenecks in food safety, harvesting and processing, environmental sustainability, regulation, and consumer behaviour. As similar hurdles exist for farmed edible insects, and are currently being addressed in research agendas, we argue that earthworm farming could benefit from the knowledge and frameworks that are being generated for insects. For instance, food safety procedures developed in insect farming could be adapted to earthworm farming to reduce the risk of contamination with heavy metals, pesticides, pharmaceuticals and microbial pathogens (Finke et al., 2015; van der Fels-Klerx et al., 2018). This includes screening methods, pre-processing treatments for contaminated residual streams, and drying and processing equipment.
Other bottlenecks for up-scaling earthworm farming are linked to the processing steps described by Medina and Araque (1999), including harvesting, washing and voiding, killing and preservation. Harvesting presents a technical challenge because the trommel-sieves used for separating mature earthworms from vermicompost can become clogged if the vermicompost is too wet. Achieving optimal moisture is therefore crucial and may be difficult when heterogeneous residual streams are used. Harvested earthworms, as mentioned above, should be voided to increase protein content, particularly if mineral particles are present in the feed material. This process involves submerging harvested earthworms at around 20 °C for 24-48 hours in water with a low salt content, as high salt contents would kill the worms (Sherman, 2018). The water also needs to be aerated by a pump to maintain sufficient oxygen levels for earthworms to breathe through their skin. This process may be challenging and water-intensive with large volumes of earthworms. If no mineral particles are present in the feed, it may be possible and safe to process them without voiding of the gut. Next, the earthworms need to be killed and processed to meet food safety standards. Killing is often done by freezing, which is energy-intensive. Alternative options may be osmotic dehydration by salt or suffocation in CO2. Ethical concerns should be considered in investigating these options. Finally, the dead earthworms need to be processed or preserved for food purposes, which has important implications for energy-use, nutritional quality and food safety. Oven-drying or freeze-drying are the most common practices for the preparation of earthworm meal. Freeze-drying of earthworms, as compared to oven drying, preserves unsaturated omega-3 fatty acids (Gunya et al., 2016a), but the high energy-use involved affects the overall sustainability of earthworms as food (Tedesco et al., 2019). Oven-, microwave-, or sun-drying (Suárez-Hernández et al., 2016a), smoking (Paoletti et al., 2003), ensiling (Ortega Cerrilla et al., 1996b), or preservation of earthworms in salt may present less energy-intensive alternatives. Direct fresh processing of earthworms into sausages or burger patties, for instance, may be feasible with short producer-to-consumer distances for products which are sterilized by cooking before consumption. Depending on the feed material, earthworms may be contaminated with microbial pathogens and can transmit tapeworms and nematodes pathogenic to birds and mammals (Swati and Hait, 2018; Edwards and Arancon, 2022). Vermicomposting reduces microbial contamination by different mechanisms (Swati and Hait, 2018) and processing methods presenting a kill-step, such as oven-drying, microwave-drying, or cooking can further reduce contamination (Conti et al., 2019; Tedesco et al., 2020). Processing is also important for changes in consumer behaviour, as only an appealing product will convince the consumer. Information and awareness are key variables for earthworms to be accepted as an alternative protein source in human diets (Conti et al., 2018; Russo et al., 2020).
Finally, it is necessary to expand our knowledge on the environmental sustainability of earthworm farming. This includes identifying which combinations of earthworm species with residual streams are most productive, quantifying greenhouse gas emissions of these species-feed combinations, determining optimal substrate-to-earthworm ratios for protein production, and quantifying energy, water, N and P use (Tedesco et al., 2019). The frameworks developed for farmed insects (Dortmans et al., 2017; Mertenat et al., 2019; Smetana et al., 2021) can also be useful in this case.
11 Conclusion
We have demonstrated that earthworms are rich in protein with a complete profile of essential amino acids, and contain important fatty acids, minerals and vitamins. This composition indicates the substantial potential of earthworms as a future food from a nutritional standpoint. We argue that earthworms, given their capacity for upcycling organic residual streams to edible protein and valuable compost, should play a role in the transition towards circular food systems. Compared to edible insects, earthworms may provide several sustainability advantages in terms of energy-use, feed material, and the occurrence of diseases. Further research is necessary to optimize the productivity and nutritional composition of commonly farmed earthworm species feeding on different materials. In addition, greenhouse gas emissions and nutrient flows should be quantified to inform a sustainability assessment of earthworm farming as a protein source for human nutrition.
Corresponding author; e-mail: enno.sonntag@thuenen.de
Supplementary material
Supplementary material is available online at: https://doi.org/10.6084/m9.figshare.24518659
Acknowledgements
The authors declare no conflict of interest. This study was funded by the Johann Heinrich von Thuenen Institute, German Federal Research Institute for Rural Areas, Forestry and Fisheries.
References
Agunbiadi, J.A., Adeyemi, O.A., Idowu, O.R., Ajayi, O.A., Awojobi, H.A. and Eniolorunda, O.O., 2010. Nutritional and histopathological assessment of earthworm meal as dietary protein source for broiler starters. In: Proceedings of Tropentag 2010, Zurich, p. 458.
Albro, P.W., Corbett, J.T. and Schroeder, J.L., 1993. Endogenous lipids of the earthworm Lumbricus terrestris. Biochemistry and Cell Biology 71: 220-221. https://doi.org/10.1139/o93-033
Albro, P.W., Schroeder, J.L. and Corbett, J.T., 1992. Lipids of the earthworm Lumbricus terrestris. Lipids 27: 136-143. https://doi.org/10.1007/BF02535813
Alcı́var-Cedeño, U., Dueñas-Rivadeneira, A., Sacon-Vera, E., Bravo-Sánchez, L. and Villanueva-Ramos, G., 2016. Influencia de los tipos de secado para la obtención de harina de lombriz roja californiana (Eisenia foetida) a escala piloto. Tecnologı́a Quı́mica 36: 187-196.
Ansari, A.A. and Sitaram, K., 2011. An investigation into the anti-microbial and anti-fungal properties of earthworm powder obtained from Eisenia fetida. American Journal of Food Technology 6: 329-335.
Arévalo-Pinedo, A., Vásquez-Ribeiro, O. and Sallés Arévalo, Z.D., 2004. Obtención, evaluación fı́sico-quı́mica y almacenamiento de la “harina de lombriz” de tierra (Eisenia foetida). Alimentaria: Revista de tecnologı́a e higiene de los alimentos 358: 75-78.
Ayaz, S.M. and Vadher, K.H., 2020. Evaluation of the nutritional quality of selected dietary ingredients for mud crab Scylla serrata of Suarashtra region in Gujarat, India. Journal of Applied and Natural Science 12: 288-291. https://doi.org/10.31018/jans.v12i3.2243
Ayieko, M.A., Kinyuru, J.N., Makhado, R., Potgieter, M., Tshikudo, P., Mawela, K., Maluleke-Nyathela, H., Oonincx, D.J. and Cloutier, J., 2015. Locusts and grasshoppers (Orthoptera). In: Cloutier, J. (ed.) Edible insects in Africa: an introduction to finding, using and eating insects. Wageningen Academic Publishers, Wageningen, The Netehrlands, pp. 45-54.
Babiker, M.S., 2012. Chemical composition of some non-conventional and local feed resources for poultry in Sudan. International Journal of Poultry Science 11: 283-287. https://doi.org/10.3923/ijps.2012.283.287
Bahadori, Z., Esmaylzadeh, L. and Karimi-Torshizi, M.A., 2015. The effect of earthworm (Eisenia fetida) and vermihumus meal in diet on broilers chicken efficiency and carcass components. Biological Forum – An International Journal 7: 998-1005.
Barker, D., Fitzpatrick, M.P. and Dierenfeld, E.S., 1998. Nutrient composition of selected whole invertebrates. Zoo Biology 17: 123-134. https://doi.org/10.1002/(SICI)1098-2361(1998)17:2<123:AID-ZOO7>3.0.CO;2-B
Beg, M.M., Mandal, B. and Moulick, S., 2016. Potential of earthworm meal as a replacement of fish meal for Indian major carps. International Journal of Fisheries and Aquatic Studies 4: 357-361.
Blouin, M., Hodson, M.E., Delgado, E.A., Baker, G., Brussaard, L., Butt, K.R., Dai, J., Dendooven, L., Peres, G., Tondoh, J.E., Cluzeau, D. and Brun, J.-J., 2013. A review of earthworm impact on soil function and ecosystem services. European Journal of Soil Science 64: 161-182. https://doi.org/10.1111/ejss.12025
Bosch, G., Oonincx, D., Jordan, H.R., Zhang, J., van Loon, J., van Huis, A. and Tomberlin, J.K., 2020. Standardisation of quantitative resource conversion studies with black soldier fly larvae. Journal of Insects as Food and Feed 6: 95-109. https://doi.org/10.3920/JIFF2019.0004
Bou-Maroun, E., Loupiac, C., Loison, A., Rollin, B., Cayot, P., Cayot, N., Marquez, E. and Medina, A.L., 2013. Impact of preparation process on the protein structure and on the volatile compounds in Eisenia foetida protein powders. Food and Nutrition Sciences 4: 1175-1183. https://doi.org/10.4236/fns.2013.411151
Bouché, M., 1971. Relations entre les structures spatiales et fonctionnelles des écosystèmes illustrées par le rôle pédobiologique des vers de terre. In: Pesson, P. (ed.) La vie des sols. Gauthier-Villars, Paris, France, pp. 187-209.
Bouché, M., 1977. Strategies lombriciennes. Soil Organisms as Components of Ecosystems 25: 122-132.
Boulos, S., Tännler, A. and Nyström, L., 2020. Nitrogen-to-protein conversion factors for edible insects on the Swiss market: T. molitor, A. domesticus, and L. migratoria. Frontiers in Nutrition 7: 89. https://doi.org/10.3389/fnut.2020.00089
Cappellozza, S., Leonardi, M.G., Savoldelli, S., Carminati, D., Rizzolo, A., Cortellino, G., Terova, G., Moretto, E., Badaile, A., Concheri, G., Saviane, A., Bruno, D., Bonelli, M., Caccia, S., Casartelli, M. and Tettamanti, G., 2019. A first attempt to produce proteins from insects by means of a circular economy. Animals 9: 278. https://doi.org/10.3390/ani9050278
Castro-Bedriñana, J., Chirinos-Peinado, D. and Sosa-Blas, H., 2020. Digestibility, digestible and metabolizable energy of earthworm meal (Eisenia foetida) included in two levels in Guinea pigs (Cavia porcellus). Advances in Science, Technology and Engineering Systems Journal 5: 171-177. https://doi.org/10.25046/aj050323
Cayot, N., Cayot, P., Bou-Maroun, E., Laboure, H., Abad-Romero, B., Pernin, K., Seller-Alvarez, N., Hernández, A.V., Marquez, E. and Medina, A.L., 2009. Physico-chemical characterisation of a non-conventional food protein source from earthworms and sensory impact in arepas. International Journal of Food Science & Technology 44: 2303-2313. https://doi.org/10.1111/j.1365-2621.2009.02074.x
Cerbulis, J. and Taylor, M.W., 1969. Neutral lipid and fatty acid composition of earthworms (Lumbricus terrestris). Lipids 4: 363-368. https://doi.org/10.1007/BF02531007
Chakraborty, P., Islam, M.R., Hossain, M.A., Fatema, U.K., Shaha, D.C., Sarker, M.S.A. and Akter, T., 2021. Earthworm meal (Perionyx excavatus) as an alternative protein source to fish meal in feed for juvenile butter catfish (Ompok pabda). Aquaculture International 29: 2119-2129. https://doi.org/10.1007/s10499-021-00737-y
Changguo, X., Pingjiu, Z., Genxing, P., Duosheng, Q. and Qiuhua, C., 2006. Changes in diversity, protein content, and amino acid composition of earthworms from a paddy soil under different long-term fertilizations in the Tai Lake Region, China. Acta Ecologica Sinica 26: 1667-1674.
de Chaves, R.C., Paula, R.Q., Gücker, B., Marriel, I.E., Teixeira, A.O. and Boëchat, I.G., 2015. An alternative fish feed based on earthworm and fruit meals for tilapia and carp postlarvae. Revista Brasileira de Biociências 13: 15-24.
Chia, S.Y., Tanga, C.M., Osuga, I.M., Cheseto, X., Ekesi, S., Dicke, M. and van Loon, J.J., 2020. Nutritional composition of black soldier fly larvae feeding on agro-industrial by-products. Entomologia Experimentalis et Applicata 168: 472-481. https://doi.org/10.1111/eea.12940
Chilmawati, D., Suminto, Subandiyono and Harwanto, D., 2021. Performance of growth, nutrition value, total carotene, EPA, and DHA in eel (Anguilla bicolor) in the culture with enrichment of earthworm (Lumbricus sp.) flour. AACL Bioflux 14: 1570-1580.
Chiu, S.-T., Wong, S.-L., Shiu, Y.-L., Chiu, C.-H., Guei, W.-C. and Liu, C.-H., 2016. Using a fermented mixture of soybean meal and earthworm meal to replace fish meal in the diet of white shrimp, Penaeus vannamei (Boone). Aquaculture Research 47: 3489-3500. https://doi.org/10.1111/are.12799
Conti, C., Castrica, M., Balzaretti, C.M. and Tedesco, D.E.A., 2019. Edible earthworms in a food safety perspective: preliminary data. Italian Journal of Food Safety 8: 7695. https://doi.org/10.4081/ijfs.2019.7695
Conti, C., Costa, A., Balzaretti, C., Russo, V. and Tedesco, D., 2018. Survey on food preferences of university students: from tradition to new food customs? Agriculture 8: 155. https://doi.org/10.3390/agriculture8100155
Cortes Ortiz, J.A., Ruiz, A.T., Morales-Ramos, J.A., Thomas, M., Rojas, M.G., Tomberlin, J.K., Yi, L., Han, R., Giroud, L. and Jullien, R.L., 2016. Chapter 6 – Insect mass production technologies. In: Dossey, A.T., Morales-Ramos, J.A. and Rojas, M.G. (eds.) Insects as sustainable food ingredients: production, processing and food applications. Academic Press, Cambridge, MA, USA, pp. 153-201.
Da, C.T., Lundh, T. and Lindberg, J.E., 2013. Digestibility of dietary components and amino acids in animal and plant protein feed ingredients in striped catfish (Pangasianodon hypophthalmus) fingerlings. Aquaculture Nutrition 19: 741-750. https://doi.org/10.1111/anu.12021
Dai, J., Becquer, T., Rouiller, J.H., Reversat, G., Bernhard-Reversat, F., Nahmani, J. and Lavelle, P., 2004. Heavy metal accumulation by two earthworm species and its relationship to total and DTPA-extractable metals in soils. Soil Biology and Biochemistry 36: 91-98. https://doi.org/10.1016/j.soilbio.2003.09.001
Das, U.N., 2006. Essential fatty acids: biochemistry, physiology and pathology. Biotechnology Journal 1: 420-439. https://doi.org/10.1002/biot.200600012
Dedeke, G.A., Owa, S.O. and Olurin, K.B., 2010a. Amino acid profile of four earthworms species from Nigeria. Agriculture and Biology Journal of North America 1: 97-102.
Dedeke, G.A., Owa, S.O. and Olurin, K.B., 2010b. Macromineral profile of four species of earthworm Hyperiodrilus africanus, Eudrilus eugeniae, Libryodrilus violaceous and Alma mansoni from Nigeria. Current Research Journal of Biological Sciences 2: 103-106.
Dedeke, G.A., Owa, S.O., Olurin, K.B., Akinfe, A.O. and Awotedu, O.O., 2013. Partial replacement of fish meal by earthworm meal (Libyodrilus violaceus) in diets for African catfish, Clarias gariepinus. International Journal of Fisheries and Aquaculture 5: 229-233.
Dierenfeld, E.S. and King, J., 2008. Digestibility and mineral availability of Phoenix worms, Hermetia illucens, ingested by mountain chicken frogs, Leptodactylus fallax. Journal of Herpetological Medicine and Surgery 18: 100-105. https://doi.org/10.5818/1529-9651.18.3-4.100
Ding, S., Lin, X. and He, S., 2019. Earthworms: a source of protein. Journal of Food Science and Engineering 9: 159-170. https://doi.org/10.17265/2159-5828/2019.05.001
Djissou, A.S.M., Adjahouinou, D.C., Koshio, S. and Fiogbe, E.D., 2016. Complete replacement of fish meal by other animal protein sources on growth performance of Clarias gariepinus fingerlings. International Aquatic Research 8: 333-341. https://doi.org/10.1007/s40071-016-0146-x
Dobermann, D., Swift, J.A. and Field, L.M., 2017. Opportunities and hurdles of edible insects for food and feed. Nutrition Bulletin 42: 293-308. https://doi.org/10.1111/nbu.12291
Domı́nguez, J., Sanchez-Hernandez, J.C. and Lores, M., 2017. 3 – Vermicomposting of winemaking by-products. In: Galanakis, C.M. (ed.) Handbook of grape processing by-products: sustainable solutions. Elsevier Science, San Diego, CA, USA, pp. 55-78.
Dong, X.-H., Guo, Y.-X., Ye, J.-D., Song, W.-D., Huang, X.-H. and Wang, H., 2010. Apparent digestibility of selected feed ingredients in diets for juvenile hybrid tilapia, Oreochromis niloticus × Oreochromis aureus. Aquaculture Research 41: 1356-1364. https://doi.org/10.1111/j.1365-2109.2009.02424.x
Dortmans, B., Diener, S., Verstappen, B. and Zurbrügg, C., 2017. Black soldier fly biowaste processing: a step-by-step guide. Eawag – Swiss Federal Institute of Aquatic Science and Technology, Dübendorf, Switzerland.
Douglas, A.E., 2017. The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally acquired genes. Current Opinion in Insect Science 23: 65-69. https://doi.org/10.1016/j.cois.2017.07.012
Drilobase Project, 2013. DriloBASE Taxo. Available at: http://taxo.drilobase.org
Dynes, R.A., 2003a. Earthworms: technology information to enable the development of earthworm production, a report for the Rural Industries Research and Development Corporation. Rural Industries Research and Development Corporation, Canberra, Australia, p. 33.
Dynes, R.A., 2003b. Earthworms: technology information to enable the development of earthworm production: a report for the Rural Industries Research and Development Corporation. Rural Industries Research and Development Corporation, Barton, A.C.T.
Dzepe, D., Magatsing, O., Kuietche, H.M., Meutchieye, F., Nana, P., Tchuinkam, T. and Djouaka, R., 2021. Recycling organic wastes using black soldier fly and house fly larvae as broiler feed. Circular Economy and Sustainability 1: 895-906. https://doi.org/10.1007/s43615-021-00038-9
Edwards, C.A., 1983. Production of earthworm protein for animal feed from potatoe waste. In: Ledward, D.A., Taylor, A.J. and Lawrie, R.A. (eds.) Upgrading waste for feeds and food: proceedings of previous easter schools in agricultural science. Elsevier, Amsterdam, The Netherlands, pp. 153-162.
Edwards, C.A., 1985. Production of feed protein from animal waste by earthworms. Philosophical Transactions of the Royal Society of London B, Biological Sciences 310: 299-307. https://doi.org/10.1098/rstb.1985.0120
Edwards, C.A. and Arancon, N.Q., 2022. Earthworms as pests and benefactors. In: Edwards, C.A. and Arancon, N.Q. (eds.) Biology and ecology ofearthworms. Springer, New York, NY, USA, pp. 335-370.
Edwards, C.A., Arancon, N.Q. and Sherman, R.L. (eds.), 2011. Vermiculture technology: earthworms, organic wastes, and environmental management. CRC Press, Boca Raton, FL, USA, p. 578.
Edwards, C.A. and Dominguez, J., 2011. Biology and ecology of earthworm species used for vermicomposting. In: Edwards, C.A., Arancon, N.Q. and Sherman, R.L. (eds.) Vermiculture technology: earthworms, organic wastes, and environmental management. CRC Press, Boca Raton, FL, USA, pp. 27-40.
EFSA Scientific Committee, 2015. Risk profile related to production and consumption of insects as food and feed. EFSA Journal 13: 4257. https://doi.org/10.2903/j.efsa.2015.4257
Finke, M.D., 2002. Complete nutrient composition of commercially raised invertebrates used as food for insectivores. Zoo Biology 21: 269-285. https://doi.org/10.1002/zoo.10031
Finke, M.D., 2007. Estimate of chitin in raw whole insects. Zoo Biology 26: 105-115. https://doi.org/10.1002/zoo.20123
Finke, M.D., 2013. Complete nutrient content of four species of feeder insects. Zoo Biology 32: 27-36. https://doi.org/10.1002/zoo.21012
Finke, M.D., Rojo, S., Roos, N., van Huis, A. and Yen, A.L., 2015. The European Food Safety Authority scientific opinion on a risk profile related to production and consumption of insects as food and feed. Journal of Insects as Food and Feed 1: 245-247. https://doi.org/10.3920/jiff2015.x006
Fisher, C., 1988. The nutritional value of earthworm meal for poultry. In: Edwards, C.A. and Neuhauser, E.F. (eds.) Earthworms in waste and environmental management. SPB Academic Publishing, The Hague, The Netherlands, pp. 181-192.
Flores, M.T. and Alvira, P., 1987. Composicion quimico-bromatologica y proporaón de aminoacidos de la harina de la lombriz de tierra (E. foetida Sav. y L. rubellus Hoff.). Anales de Edafologia y Agrobiologia 46: 758-798.
Fosgate, O.T. and Babb, M.R., 1972. Biodegradation of animal waste by Lumbricus terrestris. Journal of Dairy Science 55: 870-872. https://doi.org/10.3168/jds.s0022-0302(72)85586-3
French, C.E., Liscinsky, S.A. and Miller, D.R., 1957. Nutrient composition of earthworms. The Journal of Wildlife Management 21: 348. https://doi.org/10.2307/3796557
Garcı́a, D.E., Cova, L.J., Castro, A.R., Medina, M.G. and Palma, J.R., 2009. Effect of the nutritional substrate in the chemical composition and nutritives value of red worm (Eisenia spp.) meal. Revista Cientı́fica 19: 55-62.
Garcı́a, M.D., Oruña, L., Domı́nguez, H. and Martı́nez, V., 2005. Evaluación de la calidad proteica de harina de lombriz (Eisenia foetida) en ratas en crecimiento. Revista Cubana de Ciencia Agrı́cola 39: 333-338.
Garczyńska, M., Kostecka, J., Pączka, G., Mazur-Pączka, A., Cebulak, T. and Butt, K.R., 2023. Chemical composition of earthworm (Dendrobaena veneta Rosa) biomass is suitable as an alternative protein source. International Journal of Environmental Research and Public Health 20: 3108. https://doi.org/10.3390/ijerph20043108
Gianotten, N., Soetemans, L. and Bastiaens, L., 2020. Agri-food side-stream inclusions in the diet of Alphitobius diaperinus. Part 1: impact on larvae growth performance parameters. Insects 11: 79. https://doi.org/10.3390/insects11020079
Gkinali, A.-A., Matsakidou, A., Vasileiou, E. and Paraskevopoulou, A., 2022. Potentiality of Tenebrio molitor larva-based ingredients for the food industry: a review. Trends in Food Science & Technology 119: 495-507. https://doi.org/10.1016/j.tifs.2021.11.024
Graff, O., 1981. Preliminary experiment of vermicomposting of different waste materials using Eudrilus eugeniae Kinberg. In: Proceedings of the Workshop on the Role of Earthworms in the Stabilization of Organic Residues, Kalamazoo, Michigan, April 9-12, 1980, pp. 179-191.
Graff, O., 1982. Vergleich der Regenwurmarten Eisenia foetida und Eudrilus eugeniae hinsichtlich ihrer Eignung zur Proteingewinnung aus Abfallstoffen. Pedobiologia 23: 277-282.
Grdiša, M., Gršić, K. and Grdiša, M.D., 2013. Earthworms – role in soil fertility to the use in medicine and as a food. Invertebrate Survival Journal 10: 38-45.
Grimm, D. and Wösten, H.A.B., 2018. Mushroom cultivation in the circular economy. Applied Microbiology and Biotechnology 102: 7795-7803. https://doi.org/10.1007/s00253-018-9226-8
Guerrero, R.D., 1983. The culture and use of Perionyx excavatus as a protein resource in the Philippines. In: Satchell, J.E. (ed.) Earthworm ecology: from Darwin to vermiculture. Springer, Dordrecht, The Netherlands, pp. 309-313.
Guerrero, R.D., Guerrero, L.A. and Cargado, A.K., 1984. Studies on the culture of the earthworm, Eudrilus euginae, and its use as feed for Macrobrachium idella and fertilizer source for Brassica compensis. Transactions of the National Academy of Science and Technology Philippines 6: 33-40.
Gunya, B., Masika, P.J., Hugo, A. and Muchenje, V., 2016a. Nutrient composition and fatty acid profiles of oven-dried and freeze-dried earthworm Eisenia foetida. Journal of Food and Nutrition Research 4: 343-348. https://doi.org/10.12691/jfnr-4-6-1
Gunya, B., Masika, P.J., Hugo, A. and Muchenje, V., 2016b. Nutrient composition and fatty acid profiles of oven-dried and freeze-dried earthworm Eisenia foetida. Journal of Food and Nutrition Research 4: 343-348. https://doi.org/10.12691/jfnr-4-6-1
Gunya, B., Muchenje, V. and Masika, P.J., 2018. The effect of Eisenia foetida meal as a protein source on sensory attributes of broiler meat. Livestock Research for Rural Development 30.
Habashy, M., 2012. 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. Egyptian Journal of Aquatic Biology and Fisheries 16: 105-114. https://ddoi.org/10.21608/ejabf.2012.2116
Halloran, A., Roos, N., Eilenberg, J., Cerutti, A. and Bruun, S., 2016. Life cycle assessment of edible insects for food protein: a review. Agronomy for Sustainable Development 36: 57. https://doi.org/10.1007/s13593-016-0392-8
Hambræus, L., 2014. Protein and amino acids in human nutrition. In: Caplan, M.J. (ed.) Reference module in biomedical sciences. Elsevier, Amsterdam, The Netherlands.
Hamid, S.N.I.N., Abdullah, M.F., Zakaria, Z., Yusof, S.H.M. and Abdullah, R., 2016. Formulation of fish feed with optimum protein-bound lysine for African catfish (Clarias gariepinus) Fingerlings. Procedia Engineering 148: 361-369. https://doi.org/10.1016/j.proeng.2016.06.468
Hansen, R.P. and Czochanska, Z., 1975. The fatty acid composition of the lipids of earthworms. Journal of the Science of Food and Agriculture 26: 961-971. https://doi.org/10.1002/jsfa.2740260713
Harinarayan, C.V., Akhila, H. and Shanthisree, E., 2021. Modern India and dietary calcium deficiency – half a century nutrition data – retrospect-introspect and the road ahead. Frontiers in Endocrinology 12: 583654. https://doi.org/10.3389/fendo.2021.583654
Hartenstein, R., 1981. Use of Eisenia foetida in organic recycling based on laboratory experiments. In: Proceedings of the Workshop on the Role of Earthworms in the Stabilization of Organic Residues, Kalamazoo, Michigan, April 9-12, 1980, pp. 155-165.
Hartenstein, R., Leaf, A.L., Neuhauser, E.F. and Bickelhaupt, D.H., 1980a. Composition of the earthworm Eisenia foetida (Savigny) and assimilation of 15 elements from sludge during growth. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology 66: 187-192. https://doi.org/10.1016/0306-4492(80)90124-0
Hartenstein, R., Neuhauser, E.F. and Collier, J., 1980b. Accumulation of heavy metals in the earthworm Eisenia foetida. Journal of Environmental Quality 9: 23-26. https://doi.org/10.2134/jeq1980.00472425000900010007x
Harwood, M.B., 1976. Recovery of protein from poultry waste by earthworm. In: Proceedings of the Australasian Poultry Stockfeed Convention, Sydney, pp. 138-143.
Harwood, M.B. and Sabine, J.R., 1978. The nutritive value of worm meal. In: Proceedings of the second Australasian poultry stockfeed convention, Sydney, pp. 164-171.
Hasanuzzaman, A.F.M., Hossian, S.Z. and Das, M., 2010. Nutritional potentiality of earthworm (Perionyx excavatus) for substituting fishmeal used in local feed company in Bangladesh. Mesopotamian Journal of Marine Sciences 25: 134-139. https://doi.org/10.58629/mjms.v25i2.196
Herawati, V.E., Nugroho, R.A., Pinandoyo, Hutabarat, J., Prayitno, B. and Karnaradjasa, O., 2018. The growth performance and nutrient quality of Asian swamp eel Monopterus albus in central Java Indonesia in a freshwater aquaculture system with different feeds. Journal of Aquatic Food Product Technology 27: 658-666. https://doi.org/10.1080/10498850.2018.1483990
Herrero, M., Thornton, P.K., Mason-D’Croz, D., Palmer, J., Benton, T.G., Bodirsky, B.L., Bogard, J.R., Hall, A., Lee, B., Nyborg, K., Pradhan, P., Bonnett, G.D., Bryan, B.A., Campbell, B.M., Christensen, S., Clark, M., Cook, M.T., de Boer, I.J.M., Downs, C., Dizyee, K., Folberth, C., Godde, C.M., Gerber, J.S., Grundy, M., Havlik, P., Jarvis, A., King, R., Loboguerrero, A.M., Lopes, M.A., McIntyre, C.L., Naylor, R., Navarro, J., Obersteiner, M., Parodi, A., Peoples, M.B., Pikaar, I., Popp, A., Rockström, J., Robertson, M.J., Smith, P., Stehfest, E., Swain, S.M., Valin, H., van Wijk, M., van Zanten, H.H.E., Vermeulen, S., Vervoort, J. and West, P.C., 2020. Innovation can accelerate the transition towards a sustainable food system. Nature Food 1: 266-272. https://doi.org/10.1038/s43016-020-0074-1
Hilton, J.W., 1983. Potential of freeze-dried worm meal as a replacement for fish meal in trout diet formulaions. Aquaculture 32: 277-283. https://doi.org/10.1016/0044-8486(83)90224-7
Holmstrup, M., Sørensen, L.I., Bindesbøl, A.-M. and Hedlund, K., 2007. Cold acclimation and lipid composition in the earthworm Dendrobaena octaedra. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 147: 911-919. https://doi.org/10.1016/j.cbpa.2007.02.019
Hong, J., Han, T. and Kim, Y.Y., 2020. Mealworm (Tenebrio molitor larvae) as an alternative protein source for monogastric animal: a review. Animals 10: 2068. https://doi.org/10.3390/ani10112068
Hopkins, I., Newman, L.P., Gill, H. and Danaher, J., 2021. The influence of food waste rearing substrates on black soldier fly larvae protein composition: a systematic review. Insects 12: 608. https://doi.org/10.3390/insects12070608
Hřebečková, T., Wiesnerová, L. and Hanč, A., 2020. Change in agrochemical and biochemical parameters during the laboratory vermicomposting of spent mushroom substrate after cultivation of Pleurotus ostreatus. The Science of the Total Environment 739: 140085. https://doi.org/10.1016/j.scitotenv.2020.140085
Ibáñez, I.A., Herrera, C.A., Velásquez, L.A. and Hebel, P., 1993. Nutritional and toxicological evaluation on rats of earthworm (Eisenia fetida) meal as protein source for animal feed. Animal Feed Science and Technology 42: 165-172. https://doi.org/10.1016/0377-8401(93)90031-e
Ireland, M.P., 1979. Metal accumulation by the earthworms Lumbricus rubellus, Dendrobaena veneta and Eiseniella tetraedra living in heavy metal polluted sites. Environmental Pollution 19: 201-206. https://doi.org/10.1016/0013-9327(79)90041-7
Isea-Leon, F., Acosta-Balbias, V., Rial-Betancoutd, L.B., Medina-Gallardo, A.L. and Celestin, B.M., 2019. Evaluation of the fatty acid composition of earthworm Eisenia andrei meal as an alternative lipid source for fish feed. Journal of Food and Nutrition Research 7: 696-700. https://doi.org/10.12691/jfnr-7-10-2
Istiqomah, L., Sakti, A.A., Suryani, A.E., Karimy, M.F., Anggraeni, A.S. and Herdian, H., 2017. Effect of feed supplement containing earthworm meal (Lumbricus rubellus) on production performance of quail (Coturnix coturnix japonica). IOP Conference Series: Earth and Environmental Science 101: 12032. https://doi.org/10.1088/1755-1315/101/1/012032
Istiqomah, L., Sofyan, A., Damayanti, E. and Julendra, H., 2009. Amino acid profile of earthworm and earthworm meal (Lumbricus rubellus) for animal feedstuff. Journal of the Indonesian Tropical Animal Agriculture 34: 253-257. https://doi.org/10.14710/jitaa.34.4.253-257
Janković, L.J., Petrujkić, B., Aleksić, N., Vučinić, M., Teodorović, R., Karabasil, N., Relić, R., Drašković, V. and Nenadović, K., 2020. Caracass production and internal organs of broiler fed earthworm (Lumbricus rubellus) meal. Journal of the Hellenic Veterinary Medical Society 71: 2031-2040.
Janković, L.J., Radenković-Damnjanović, B., Vucinić, M., Sefer, D., Teodorović, R., Dordević, M. and Radisavljević, K., 2015. Effects of fish meal replacement by red earthworm (lumbricus rubellus) meal on broilers performance and health. Acta Veterinaria 65: 271-286. https://doi.org/10.1515/acve-2015-0023
Janssen, R.H., Vincken, J.-P., van den Broek, L.A.M., Fogliano, V. and Lakemond, C.M.M., 2017. Nitrogen-to-protein conversion factors for three edible insects: Tenebrio molitor, Alphitobius diaperinus, and Hermetia illucens. Journal of Agricultural and Food Chemistry 65: 2275-2278. https://doi.org/10.1021/acs.jafc.7b00471
Jatmiko, P.C., Madinah, N.A., Agustono and Nurhajati, T., 2018. The effect of earthworms (Lumbricus rubellus) in feed formulation on growth and retention of eel (Anguilla bicolor). IOP Conference Series: Earth and Environmental Science 137: 12033. https://doi.org/10.1088/1755-1315/137/1/012033
Kale, R.D. and Bano, K., 1988. Earthworm cultivation and culturing techniques for production of Vee Comp 83 E UAS* and Vee Meal 83 P AUS**. Mysore Journal of Agricultural Sciences 22: 339-344.
Karabulut, H.A., Kurtoglu, I.Z., Yuksek, T. and Bayraktar, Z., 2020. The investigation of the possibility of using red California earthworm (Eisenia fetida) meal as an alternative protein source in rainbow trout (Oncorhynchus mykiss) diet. Fresenius Environmental Bulletin 29: 2951-2959.
Kaur, N., Chugh, V. and Gupta, A.K., 2014. Essential fatty acids as functional components of foods – a review. Journal of Food Science and Technology 51: 2289-2303. https://doi.org/10.1007/s13197-012-0677-0
Köhler, R., Kariuki, L., Lambert, C. and Biesalski, H.K., 2019. Protein, amino acid and mineral composition of some edible insects from Thailand. Journal of Asia-Pacific Entomology 22: 372-378. https://doi.org/10.1016/j.aspen.2019.02.002
Koreleski, J., Rys, R., Kubicz, M., Górska-Matusiak, Z. and Gawlik, Z., 1994. Nutritional value of California earthworm meal depending on the type of substrate and drying temperature. Roczniki Naukowe Zootechniki 21: 205-214.
Kostecka, J., Garczyńska, M., Pączka, G. and Mazur-Pączka, A., 2022. Chemical composition of earthworm (Eisenia fetida Sav.) biomass and selected determinants for its production. Journal of Ecological Engineering 23: 169-179. https://doi.org/10.12911/22998993/149940
Kuforiji, O.O., Agunbiade, J.A., Awojobi, H.A. and Enioiorunda, O.O., 2016. Feeding value of cassava products supplemented with earthworm meal in diets of growing rabbits. Tropical Agriculture 93: 197-208.
Kumar, R., Gupta, R.K., Yadav, R., Saifi, R., Yodha, K. and Pooja, 2022. Eisenia fetida as protein source for growth enhancement of Heteropneustes fossilis. Egyptian Journal of Aquatic Biology and Fisheries 26: 577-588. https://doi.org/10.21608/ejabf.2022.234553
Kumlu, M., Beksari, A., Eroldoğan, O.T., Yılmaz, H.A., Sarıipek, M., Kınay, E. and Turchini, G.M., 2018. DHA enrichment of the red earthworm Eisenia fetida for improving its potential as dietary source for aquaculture. Aquaculture 496: 10-18. https://doi.org/10.1016/j.aquaculture.2018.07.005
Kusnadi, Prabandari, S., Syarifudin and Suyono, 2022. Potential of maggot and earthworm meals as protein sources for the growth of Nile tilapia (Oreochromis niloticus). AACL Bioflux 15: 2609-2619.
Latsamy, P. and Perston, T.R., 2007. Fly larvae, earthworms and duckweed as feeds for frogs in an integrated farming system. Livestock Research for Rural Development 20. Available at: http://www.lrrd.org/lrrd20/supplement/lats2.htm
Latunde-Dada, G.O., Yang, W. and Vera Aviles, M., 2016. In vitro iron availability from insects and sirloin beef. Journal of Agricultural and Food Chemistry 64: 8420-8424. https://doi.org/10.1021/acs.jafc.6b03286
Lawrence, R.D. and Millar, H.R., 1945. Protein content of earthworms. Nature 155: 517. https://doi.org/10.1038/155517b0
Layman, D.K. and Rodriguez, N.R., 2009. Egg protein as a source of power, strength, and energy. Nutrition Today 44: 43-48. https://doi.org/10.1097/NT.0b013e3181959cb2
Lee, H.K., Kim, H.S., Adachi, S., Ito, S., Okamoto, K. and Kametaka, M., 1988. Occurrence of unusual fatty acids in the earthworm, Lumbricus terrestris. Agricultural and Biological Chemistry 52: 2379-2380. https://doi.org/10.1271/bbb1961.52.2379
Li, L., Xu, Z., Wu, J. and Tian, G., 2010. Bioaccumulation of heavy metals in the earthworm Eisenia fetida in relation to bioavailable metal concentrations in pig manure. Bioresource Technology 101: 3430-3436. https://doi.org/10.1016/j.biortech.2009.12.085
Loan, P.P., Nhi, H.Y., Van, T.T. and Phu, T.P., 2009. Earthworm (Perionyx excavatus) as a main protein source for growing zig-zag eel (Mastacembelus armatus) in small household aquaculture-based farming system in the Mekong river delta. In: Proceedings of the international workshop: livestock, climate change and the environment.
Lourdumary, A.J.B. and Uma, K., 2013. Nutritional evaluation of earthworm powder (Lampito mauritii). Journal of Applied Poultry Research 3: 82-84. https://doi.org/10.7324/JAPS.2013.30316
Lowe, C.N., Butt, K.R. and Sherman, R.L., 2023. Chapter 21 – Current and potential benefits of mass earthworm culture. In: Morales-Ramos, J.A. (ed.) Mass production of beneficial organisms: invertebrates and entomopathogens. 2nd ed. Elsevier Science & Technology, San Diego, CA, USA, pp. 581-597.
Lu, S., Taethaisong, N., Meethip, W., Surakhunthod, J., Sinpru, B., Sroichak, T., Archa, P., Thongpea, S., Paengkoum, S., Purba, R.A.P. and Paengkoum, P., 2022. Nutritional composition of black soldier fly larvae (Hermetia illucens L.) and its potential uses as alternative protein sources in animal diets: a review. Insects 13: 831. https://doi.org/10.3390/insects13090831
Ma, W.C., 1982. Influence of soil properties and worm-related factors on the concentration of heavy metals in earthworms. Pedobiologia (German Democratic Republic) 24: 2.
Maciel-Vergara, G., Jensen, A.B., Lecocq, A. and Eilenberg, J., 2021. Diseases in edible insect rearing systems. Journal of Insects as Food and Feed 7: 621-638. https://doi.org/10.3920/JIFF2021.0024
Mahmoud, M., Musa, A., Ahmed, A.E., Ismail, M., Hassan, H., Yagoub, I. and Salih, S., 2015. Effect of dietary inclusion of earthworm meal replacing super-concentrate on broiler performance and carcass characteristics. In: Proceedings of Tropentag 2015, Berlin, September 16-18, p. 287.
Makkar, H.P., Tran, G., Heuzé, V. and Ankers, P., 2014. State-of-the-art on use of insects as animal feed. Animal Feed Science and Technology 197: 1-33. https://doi.org/10.1016/j.anifeedsci.2014.07.008
Marconi, S., Manzi, P., Pizzoferrato, L., Buscardo, E., Cerda, H., Hernandez, D.L. and Paoletti, M.G., 2002. Nutritional evaluation of terrestrial invertebrates as traditional food in Amazonia. Biotropica 34: 273-280. https://doi.org/10.1111/j.1744-7429.2002.tb00538.x
Mazac, R., Meinilä, J., Korkalo, L., Järviö, N., Jalava, M. and Tuomisto, H.L., 2022. Incorporation of novel foods in European diets can reduce global warming potential, water use and land use by over 80%. Nature Food 3: 286-293. https://doi.org/10.1038/s43016-022-00489-9
McInroy, D.M., 1971. Evaluation of the earthworm Eisenia foetida as food for man and domestic animals. Feedstuffs.
McLaughlin, J., 1971. Biochemical studies on Eisenia foetida (Svigny, 1826), the brandling worm: I. Tissue lipids and sterols. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 38: 147-163. https://doi.org/10.1016/0305-0491(71)90294-x
Medina, A.L. and Araque, J., 1999. Obtención, composición quı́mica, funcional, perfiles electroforéticos y calidad bacteriológica de la carne y harina de lombriz Eisenia faetida. Revista de la Facultad de Farmacia 37: 31-38.
Medina, A.L., Cova, J.A., Vielma, R.A., Pujic, P., Carlos, M.P. and Torres, J.V., 2003. Immunological and chemical analysis of proteins from Eisenia foetida earthworm. Food and Agricultural Immunology 15: 255-263. https://doi.org/10.1080/09540100400010084
Mekada, H., Hayashi, N., Yokota, H. and Okumura, J., 1979. Performance of growing and laying chickens fed diets containing earthworms (Eisenia foetida). Japanese Poultry Science 16: 293-297. https://doi.org/10.2141/jpsa.16.293
Mertenat, A., Diener, S. and Zurbrügg, C., 2019. Black soldier fly biowaste treatment – assessment of global warming potential. Waste Management 84: 173-181. https://doi.org/10.1016/j.wasman.2018.11.040
Mirzabaev, A., Olsson, L., Kerr, R.B., Pradhan, P., Ferre, M.G.R. and Lotze-Campen, H., 2023. Climate change and food systems. In: von Braun, J., Afsana, K., Fresco, L.O. and Hassan, M.H.A. (eds.) Science and innovations for food systems transformation. 1st ed. Springer International Publishing, Cham, Switzerland, pp. 511-529.
Mohanta, K.N., Subramanian, S. and Korikanthimath, V.S., 2013. Evaluation of different animal protein sources in formulating the diets for Blue Gourami, Trichogaster trichopterus fingerlings. Journal of Aquaculture Research and Development 4. https://doi.org/10.4172/2155-9546.1000164
Mohanta, K.N., Subramanian, S. and Korikanthimath, V.S., 2016a. Effect of different animal protein sources on growth and nutrient utilization of guppy, Poecilia reticulata fingerlings. Proceedings of the Zoological Society 69: 96-103. https://doi.org/10.1007/s12595-014-0130-7
Mohanta, K.N., Subramanian, S. and Korikanthimath, V.S., 2016b. Potential of earthworm (Eisenia foetida) as dietary protein source for rohu (Labeo rohita) advanced fry. Cogent Food & Agriculture 2: 2-3. https://doi.org/10.1080/23311932.2016.1138594
Monebi, C.O. and Ugwumba, A.A.A., 2013. Utilization of the earthworm, Eudrilus eugeniae in the diet of Heteroclarias fingerlings. International Journal of Fisheries and Aquaculture 5: 19-25. https://doi.org/10.5897/IJFA12.092
Musyoka, S.N., Liti, D.M., Erick, O.O., Meulenbroek, P. and Waidbacher, H., 2020. Using earthworm, Eisenia fetida, to bio-convert agro-industrial wastes for aquaculture nutrition. BioResources 15: 574-587.
Nalunga, A., Komakech, A.J., Jjagwe, J., Magala, H. and Lederer, J., 2021. Growth characteristics and meat quality of broiler chickens fed earthworm meal from Eudrilus eugeniae as a protein source. Livestock Science 245: 104394. https://doi.org/10.1016/j.livsci.2021.104394
Nandeesha, M.C., Srikanth, G.K., Basavaraja, N., Keshavanath, P., Varghese, T.J., Bano, K., Ray, A.K. and Kale, R.D., 1988. Influence of earthworm meal on the growth and flesh quality of common carp. Biological Wastes 26: 189-198. https://doi.org/10.1016/0269-7483(88)90165-6
Navarro, V., Rodrı́guez, C., Montero, Y. and Maylı́n, A., 1989. Evaluación biológica de la biomasa de la lombriz de tierra cubana Eudrilus eugeniae. Ciencia y Técnica en la Agricultura Ganado Porcino 12: 75-85.
Naya, Y. and Kotake, M., 1967. Untersuchung der freien Fettsäuren, der freien Sterine, der Sterinester und der Glyzeride im Regenwurm (Lumbricus spencer). Bulletin of the Chemical Society of Japan 40: 880-884. https://doi.org/10.1246/bcsj.40.880
Neuhauser, E.F., Cukic, Z.V., Malecki, M.R., Loehr, R.C. and Durkin, P.R., 1995. Bioconcentration and biokinetics of heavy metals in the earthworm. Environmental pollution (Barking, Essex 1987) 89: 293-301. https://doi.org/10.1016/0269-7491(94)00072-l
Ngoc, T.N., 2010. Development of supplemental diets for carp in Vietnamese upland ponds based on locally available resources [PhD], Universität Hohenheim, Germany.
Ngoc, T.N., Pucher, J., Becker, K. and Focken, U., 2016. Earthworm powder as an alternative protein source in diets for common carp (Cyprinus carpio L.). Aquaculture Research 47: 2917-2927. https://doi.org/10.1111/are.12743
Ngoc, T.N., Yaemkong, S., Jaipong, P., Kotham, P. and Do Anh, M., 2021. Effects of earthworm (Perionyx excavates) inclusion to the growth, feed utilization and lipid composition of common carp (Cyprinus carpio). AACL Bioflux 13: 1201-1212.
Nguyen, H., Preston, T.R., Ogle, B. and Lundh, T., 2010. Effect of earthworms as replacement for trash fish and rice field prawns on growth and survival rate of marble goby (Oxyeleotris marmoratus) and Tra catfish (Pangasius hypophthalmus). Livestock Research for Rural Development 22. Available at: http://www.lrrd.org/lrrd22/11/Nhi22204.htm
Ojha, S., Bekhit, A.E.-D., Grune, T. and Schlüter, O.K., 2021. Bioavailability of nutrients from edible insects. Current Opinion in Food Science 41: 240-248. https://doi.org/10.1016/j.cofs.2021.08.003
Oonincx, D.G. and Finke, M.D., 2021. Nutritional value of insects and ways to manipulate their composition. Journal of Insects as Food and Feed 7: 639-659. https://doi.org/10.3920/JIFF2020.0050
Oonincx, D.G., Laurent, S., Veenenbos, M.E. and van Loon, J.J.A., 2020. Dietary enrichment of edible insects with omega 3 fatty acids. Insect Science 27: 500-509. https://doi.org/10.1111/1744-7917.12669
Oonincx, D.G.A.B., van Broekhoven, S., van Huis, A. and van Loon, J.J.A., 2015. Feed conversion, survival and development, and composition of four insect species on diets composed of food by-products. PlOS ONE 10: e0144601. https://doi.org/10.1371/journal.pone.0144601
Orozco Almanza, M.S., Ortega Cerrilla, M.E. and Perez Gil Romo, F., 1988. Uso de la lombriz de tierra como suplemento proteinico en dietas para conejos. Archivos Latinoamericanos de Nutrición 38: 946-955.
Ortega Cerrilla, E., Reyes Ortigoza, A.L. and Mendoza Martı́nez, G., 1996a. Chemical composition of earthworm (Eisenia fetida and Lumbricus rubellus) silages. Archivos Latinoamericanos de Nutrición 46: 325-328.
Ortega Cerrilla, M.E., Reyes Ortigoza, A.L. and Mendoza Martı́nez, G., 1996b. Composición quı́mica de ensilados de lombrices terrestres (Eisenia fetida y Lumbricus rubellus). Archivos Latinoamericanos de Nutrición 46: 325-328.
Ovalles, J., Medina, A., Márquez, E. and Rial, L., 2017. Efecto del proceso de secado de la lombriz de tierra (Eisenia andrei) sobre el perfil aminoacı́dico de la harina determinado por cromatografı́a. Saber 29: 486-494.
Page, M.J., McKenzie, J.E., Bossuyt, P.M., Boutron, I., Hoffmann, T.C., Mulrow, C.D., Shamseer, L., Tetzlaff, J.M., Akl, E.A., Brennan, S.E., Chou, R., Glanville, J., Grimshaw, J.M., Hróbjartsson, A., Lalu, M.M., Li, T., Loder, E.W., Mayo-Wilson, E., McDonald, S., McGuinness, L.A., Stewart, L.A., Thomas, J., Tricco, A.C., Welch, V.A., Whiting, P. and Moher, D., 2021. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. British Medical Journal 372: 71. https://doi.org/10.1136/bmj.n71
Paoletti, M.G., Buscardo, E., VanderJagt, D.J., Pastuszyn, A., Pizzoferrato, L., Huang, Y.-S., Chuang, L.-T., Millson, M., Cerda, H., Torres, F. and Glew, R.H., 2003. Nutrient content of earthworms consumed by Ye’Kuana Amerindians of the Alto Orinoco of Venezuela. Proceedings of the Royal Society B: Biological Sciences 270: 249-257. https://doi.org/10.1098/rspb.2002.2141
Parodi, A., Ipema, A.F., van Zanten, H.H.E., Bolhuis, J.E., van Loon, J.J.A. and de Boer, I.J.M., 2022. Principles for the responsible use of farmed insects as livestock feed. Nature Food 3: 972-974. https://doi.org/10.1038/s43016-022-00641-5
Parodi, A., Leip, A., de Boer, I.J.M., Slegers, P.M., Ziegler, F., Temme, E.H.M., Herrero, M., Tuomisto, H., Valin, H., van Middelaar, C.E., van Loon, J.J.A. and van Zanten, H.H.E., 2018. The potential of future foods for sustainable and healthy diets. Nature Sustainability 1: 782-789. https://doi.org/10.1038/s41893-018-0189-7
Parolini, M., Ganzaroli, A. and Bacenetti, J., 2020. Earthworm as an alternative protein source in poultry and fish farming: current applications and future perspectives. The Science of the Total Environment 734: 139460. https://doi.org/10.1016/j.scitotenv.2020.139460
Paul, A., Frederich, M., Megido, R.C., Alabi, T., Malik, P., Uyttenbroeck, R., Francis, F., Blecker, C., Haubruge, E., Lognay, G. and Danthine, S., 2017. Insect fatty acids: a comparison of lipids from three Orthopterans and Tenebrio molitor L. larvae. Journal of Asia-Pacific Entomology 20: 337-340. https://doi.org/10.1016/j.aspen.2017.02.001
Pelletier, N. and Tyedmers, P., 2010. Forecasting potential global environmental costs of livestock production 2000-2050. Proceedings of the National Academy of Sciences of the United States of America 107: 18371-18374. https://doi.org/10.1073/pnas.1004659107
Pennino, M., Dierenfeld, E.S. and Behler, J.L., 1991. Retinol, α-tocopherol and proximate nutrient composition of invertebrates used as feed. International Zoo Yearbook 30: 143-149. https://dx.doi.org/10.1111/j.1748-1090.1991.tb03477.x
Pereira, J.O. and Gomes, E.F., 1995. Growth of rainbow trout fed a diet supplemented with earthworms, after chemical treatment. Aquaculture International 3: 36-42. https://doi.org/10.1007/BF00240919
Pérez-Corrı́a, K., Botello-León, A., Mauro-Félix, A.K., Rivera-Pineda, F., Viana, M.T., Cuello-Pérez, M., Botello-Rodrı́guez, A. and Martı́nez-Aguilar, Y., 2019. Chemical composition of earthworm (Eisenia foetida) co-dried with vegetable meals as an animal feed. Ciencia y Agricultura 16: 79-92. https://doi.org/10.19053/01228420.v16.n2.2019.9130
Peters, W. and Walldorf, V., 1986. Endodermal secretion of chitin in the ‘cuticle’ of the earthworm gizzard. Tissue and Cell 18: 361-374. https://doi.org/10.1016/0040-8166(86)90056-X
Petersen, S.O. and Holmstrup, M., 2000a. Temperature effects on lipid composition of the earthworms Lumbricus rubellus and Eisenia nordenskioeldi. Soil Biology and Biochemistry 32: 1787-1791. https://doi.org/10.1016/s0038-0717(00)00059-6
Petersen, S.O. and Holmstrup, M., 2000b. Temperature effects on lipid composition of the earthworms Lumbricus rubellus and Eisenia nordenskioeldi. Soil Biology and Biochemistry 32: 1787-1791. https://doi.org/10.1016/S0038-0717(00)00059-6
Phonekhampheng, O., Hung, L.T. and Lindberg, J.E., 2008. Nutritive value of potential feed resources used in Laos for African catfish (Clarias gariepinus) production. Livestock Research for Rural Development 20. Available at: http://www.lrrd.org/lrrd20/12/phon20207.htm
Piedad-Pascual, F., 1985. An evaluation of three annelids as feed ingredients in formulated diets for juvenile Penaeus monodon. Fisheries Research Journal of the Philippines 10: 9-15.
Pokarzhevskii, A.D., Zaboyev, D.P., Ganin, G.N. and Gordienko, S.A., 1997. Amino acids in earthworms: are earthworms ecosystemivorous? Soil Biology and Biochemistry 29: 559-567. https://doi.org/10.1016/s0038-0717(96)00180-0
Pucher, J., Ngoc, T.N., ThiHanhYen, T., Mayrhofer, R., El-Matbouli, M. and Focken, U., 2014. Earthworm meal as fishmeal replacement in plant based feeds for common carp in semi-intensive aquaculture in rural northern Vietnam. Turkish Journal of Fisheries and Aquatic Sciences 14: 557-565. https://doi.org/10.4194/1303-2712-v14_2_27
Purnawanto, A.M., Ahadiyat, Y.R., Iqbal, A. and Tamad, 2020. The utilization of mushroom waste substrate in producing vermicompost: the decomposer capacity of Lumbricus rubellus, Eisenia fetida and Eudrilus eugeniae. Acta Technologica Agriculturae 23: 99-104. https://doi.org/10.2478/ata-2020-0016
Rachmawati, D. and Nurhayati, D., 2022. Effect of fish meal replacement with earthworm and maggot meals on feed utilization and growth of Banana shrimp (Penaeus merguiensis). AACL Bioflux 15: 1470-1478.
Ramesh, P.T., Gunathilagaraj, K., Nagamani, B. and Kumar, M.G., 2001. Effect of earthworm meal on the growth of common carp, Cyprinus carpio L. Asian Journal of Microbiology, Biotechnology & Environmental Sciences 3: 293-295.
Rawling, M.D., Merrifield, D.L., Snellgrove, D.L., Kühlwein, H., Adams, A. and Davies, S.J., 2012. Haemato-immunological and growth response of mirror carp (Cyprinus carpio) fed a tropical earthworm meal in experimental diets. Fish & Shellfish Immunology 32: 1002-1007. https://doi.org/10.1016/j.fsi.2012.02.020
Regulation (EU) 2015/2283, 2015. EU Novel Foods Regulation.
Regulation (EU) 2023/915, 2023. on maximum levels for certain contaminants in food.
Rehman, S.u., de Castro, F., Aprile, A., Benedetti, M. and Fanizzi, F.P., 2023. Vermicompost: enhancing plant growth and combating abiotic and biotic stress. Agronomy 13: 1134. https://doi.org/10.3390/agronomy13041134
Reinecke, A.J. and Alberts, J.N., 1987. The chemical and ammo acid composition of the compost worm Eisenia fetida as potential protein source in animal feeds. Suid-Afrikaanse Tydskrif vir Natuurwetenskap en Tegnologie 6: 144-149. https://doi.org/10.4102/satnt.v6i4.960
Reinecke, A.J., Hayes, J.P. and Cilliers, S.C., 1991a. Protein quality of three different species of earthrworms. South African Journal of Animal Science 21: 99-103.
Reinecke, A.J., Hayes, J.P. and Cilliers, S.C., 1991b. Protein quality of three different species of earthrworms. South African Journal of Animal Science 21: 99-103.
Rezeaeipour, V., Nejad, O.A. and Miri, H.Y., 2014. Growth performance, blood metabolites and jejunum morphology of broiler chickens fed diets containing earthworm (Eisenia foetida) meal as a source of protein. International Journal of Advanced Biological and Biomedical Research