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Nikoletta Hetényi Department of Animal Nutrition and Clinical Dietetics, Institute for Animal Breeding, Nutrition and Laboratory Animal Science, University of Veterinary Medicine, Budapest, Hungary

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András Bersényi Department of Animal Nutrition and Clinical Dietetics, Institute for Animal Breeding, Nutrition and Laboratory Animal Science, University of Veterinary Medicine, Budapest, Hungary

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István Hullár Department of Animal Nutrition and Clinical Dietetics, Institute for Animal Breeding, Nutrition and Laboratory Animal Science, University of Veterinary Medicine, Budapest, Hungary

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Abstract

Feeding costs of farmed insects may be reduced by applying alternative nitrogen sources such as urea that can partly substitute true proteins. The aim of this study was to examine the effects of different nitrogen sources on body weight (BW) and survival rate (SR) of the Jamaican field cricket (JFC, Gryllus assimilis), the house cricket (HC, Acheta domesticus), yellow mealworm larvae (YM, Tenebrio molitor) and superworm larvae (SW, Zophobas morio). Crickets were either housed individually or in groups, and larvae were group-housed. Six isonitrogenous feeds composed of 3.52% nitrogen were designed for all four insect species using four independent replicates with micellar casein: urea proportions of 100–0%, 75–25%, 50–50%, 25–75%, 0–100% and 100% extracted soybean meal. All selected insect species were able to utilise urea. However, urea as the only nitrogen source resulted in low final BW. In the HC, the JFC, and the YM on nitrogen basis urea can replace 25% of micellar casein without having any negative effects on BW and SR in comparison to the 100% micellar casein group. In the SW, a 25% urea level did not have a significant effect on final BW, but SR decreased significantly.

Abstract

Feeding costs of farmed insects may be reduced by applying alternative nitrogen sources such as urea that can partly substitute true proteins. The aim of this study was to examine the effects of different nitrogen sources on body weight (BW) and survival rate (SR) of the Jamaican field cricket (JFC, Gryllus assimilis), the house cricket (HC, Acheta domesticus), yellow mealworm larvae (YM, Tenebrio molitor) and superworm larvae (SW, Zophobas morio). Crickets were either housed individually or in groups, and larvae were group-housed. Six isonitrogenous feeds composed of 3.52% nitrogen were designed for all four insect species using four independent replicates with micellar casein: urea proportions of 100–0%, 75–25%, 50–50%, 25–75%, 0–100% and 100% extracted soybean meal. All selected insect species were able to utilise urea. However, urea as the only nitrogen source resulted in low final BW. In the HC, the JFC, and the YM on nitrogen basis urea can replace 25% of micellar casein without having any negative effects on BW and SR in comparison to the 100% micellar casein group. In the SW, a 25% urea level did not have a significant effect on final BW, but SR decreased significantly.

Introduction

As the global population rises, the consumption of animal products is expected to increase by about 60–70% by the year 2050 (Wang et al., 2010; Makkar et al., 2014; Tilman and Clark, 2014). Insects are promising and sustainable alternative protein sources as food and feed (van Huis et al., 2013; Ribeiro et al., 2018). Insects also have the advantage of decreased impact on the environment compared to traditional livestock. Insect farming produces much less greenhouse gases and requires less land, water and feed (Oonincx and de Boer, 2012). Insects also have much lower energy requirements than mammals, while their feed conversion ratio (FCR) is like that of the monogastric farm animals (1.5–2.5 g g−1), unless their feed is very low in nutrients (Oonincx and de Boer, 2012; Melis et al., 2019; Rumbos et al., 2021). Commercial production of several insect species, including the house cricket (HC) (Acheta domesticus), the Jamaican field cricket (JFC) (Gryllus assimilis), the yellow mealworm (YM) (Tenebrio molitor) and the superworm (SW) (Zophobas morio) has already been developed (Cortes Ortiz et al., 2016; Ribeiro et al., 2018).

In the European Union, feeding legislation for farmed insects is like that of the farm animals (European Parliament and Council, 2009, 1069/2009). Insects, especially YM larvae can utilise waste and by-products low in nutrients (Cortes Ortiz et al., 2016; Morales-Ramos et al., 2020a). However, these diets tend to result in lower survival rate (SR), body weight (BW) and protein content (Oonincx et al., 2015; Bawa et al., 2020; Harsányi et al., 2020). Protein is a key macronutrient; the appropriate protein content of the feed leads to higher reproduction rate and better growth, while diets with lower protein content lead to delayed development time and decreased weight gain (Joern and Behmer, 1997; Patton, 1967). The protein content of mealworm feeds falls between 2 and 32%, but the optimal level is around 20–24% (Ramos-Elorduy et al., 2002; Morales-Ramos et al., 2020b; Kröncke et al., 2022). A protein-supplemented diet lowers the development time and improves the fecundity of YM (Morales-Ramos et al., 2013). Based on previous studies, crickets have much higher protein requirements than YM or SW larvae (Patton 1978; McCluney and Date, 2008; Lundy and Parrella, 2015; Oonincx et al., 2015; Dobermann et al., 2019). The optimum protein content in the diet of crickets should be 20–30% (Patton, 1967; Orinda et al., 2017). Feeding costs of farmed insects may be reduced by applying alternative nitrogen sources such as urea that can partly substitute true proteins. Diets of herbivorous insects (feeding on termites, cockroaches, leafhoppers, etc.) are often low in nitrogen. Symbiotic microorganisms such as Recilia dorsalis, Rhizopus oligosporus, Pseudomonas fluorescens, Serratia proteamaculans and Rahnella aquatilis can provide insect hosts with nitrogen through nitrogen fixation and nitrogenous waste recycling (Sabree et al., 2009; Ren et al., 2022; Huang et al., 2023). For example, in cockroaches, if dietary nitrogen is limited, the uric acid stored in their adipocytes is degraded into nitrogen which is then used to produce microbial protein (Ren et al., 2022).

There are 10 amino acids that are essential in arthropod diet: Ile, Leu, Lys, Met, Phe, Thr, Trp, Val, Arg and His. Tyr is a main component of sclerotin and it is required in large amounts during moulting (Cortes Ortiz et al., 2016). The non-essential amino acids that are not necessary for the growth of the YM, include Ser, Tyr, Glu and Gly. Ala, Cys, Pro and Asp are semi-essential (Davis, 1975). Thr and Trp are also limiting amino acids for the YM (John et al., 1979; Ribeiro et al., 2018). Micellar casein consists of 20% whey protein and 80% casein and is considered to be a high-quality protein source, while soy is the most used plant-origin protein source in the feed industry. This study aimed to examine whether urea as a simple nitrogen source can be utilized by the four selected insect species. If yes, we wanted to examine how it can be used for replacing the valuable protein sources like micellar casein and extracted soybean meal. The parameters measured were BW, survival rate and FCR.

Materials and methods

The insects were reared and housed in the animal house of the Institute of Animal Breeding, Nutrition and Laboratory Animal Science, University of Veterinary Medicine, Budapest, Hungary. The temperature and the relative air humidity were measured with a digital thermometer/hygrometer (TFA 30.5027.01, TFA Dostmann). The temperature and the relative air humidity of the room were 27 ± 0.4 °C and 50–60% respectively. Ethical approval was not required.

Housing and diet

In the present study, six experimentally composed isonitrogenous feeds containing 3.52% nitrogen (22% crude protein) were used (micellar casein, extracted soybean meal and corn starch adept for human consumption and bought in local shops; urea was purchased from a company distributing chemicals for laboratory purposes) to evaluate the growth performance of four different insect species. Table 1 shows the composition of the 6 isonitrogenous feeds. Nitrogen contents of feed ingredients were measured with standard methods (AOAC, 1990).

Table 1.

Ingredients of experimental isonitrogenous feeds on dry matter basis (g/100 g)

Ingredients (g)Group 1Group 2Group 3Group 4Group 5Group 6
Micellar casein28.0721.0514.047.02
Urea1.893.775.657.54
Extracted soybean meal42.2
Corn starch71.9377.0682.1987.3392.4657.8

Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50–50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

The nymphs of each cricket species and YM and SW larvae were randomly chosen and assigned to one of six experimental feed groups with four replicates/group (Table 1). The feeding experiments were carried out using 1–1.5 mm cricket nymphs kept in plastic containers. Both cricket species were either group-housed (n = 15/group, ntotal = 60/group) or individually housed (n = 1/group). Paper towel was used as bedding material and paper egg holder as a surface maximiser. Wood flakes were placed in plastic containers of water to provide footholds for the crickets to avoid drowning while consuming water. For every diet treatment, 4 replicates were obtained. Water and feed were provided ad libitum. The group-housed JFCs were kept in 206 × 156 × 83 mm containers, while the group-housed HCs were kept in 160 × 115 × 55 mm containers. Round plastic containers (66 × 20 mm) were used to provide feed and water for crickets. Individually housed crickets were kept in 85 × 55 mm round plastic containers, feed was offered in the paper egg holder and water was provided in plastic bottle cups.

YM larvae (size: 10–10.3 mm, n = 20/group, ntotal = 80/group) and SW larvae (size: 10–10.5 mm, n = 15/group, ntotal = 60/group) were reared in 140 × 100 × 75 mm plastic containers containing 50 g of feed. The feed was offered ad libitum and no water was provided as they are able the use the moisture content of the air and can survive under dry conditions (Riberio et al., 2018; Adamaki-Sotiraki et al., 2022).

Data collection and statistical analysis

BW and feed consumption were measured weekly with a digital scale (Tecator 6110). The insects were counted weekly. Means and standard deviations (SD) were calculated for each dataset. Analyses were performed using R 4.0.3. software (R Core Team, 2020). P values lower than 0.5 were evaluated as significant.

The normality of the data was tested with Quantile-Quantile Plot. Variances of the data were tested with Levene's test. One-Way ANOVA tests were performed to compare normally distributed data. Tukey's post hoc analysis was performed, if the result of the AVOVA test was significant. Non-normally distributed data were analysed with the Kruskal-Wallis rank sum test. A post-hoc Dunn Test was performed, if the Kruskal-Wallis rank sum test result was significant.

The survival rate and final mean individual BW of crickets were tested on week 4. The development of crickets was followed for 13 weeks to see whether they reach sexual maturity (as indicated by fully developed wings or ovipositors). The survival rate and final mean individual BW of YMs were tested on week 14. Data of SWs were evaluated on week 5. FCR was calculated with the following formula: FCR = amount of ingested food (g)/weight gained (g).

Results

Crickets

The initial and final BWs of both cricket species were normally distributed and had equal variances (P > 0.05). The initial BWs of cricket species did not differ significantly. The survival rates of the HCs were normally distributed and had equal variances. The survival rates of the JFCs were non-normally distributed, with equal variances. Due to frequent technical problems (moisture absorption and defecation in the feed), the feed intake of crickets could not be evaluated.

Tables 2 and 3 show the data on the HC. There was a significant difference in the final BW (P = 0.014) of group-housed crickets on week 4, between Group 5-1 (P = 0.0447) and Group 5-6 (P = 0.0213). The mean individual BW was the lowest in Group 5 and the highest in Group 6. The survival rate of the group-housed crickets was poor. The highest survival was detected in Group 5 (28.3%) and the lowest one in Group 3 (18.3%), but the survival rates did not differ significantly (P = 0.854).

Table 2.

Mean individual body weights and survival rates of group-housed house crickets on week 4

House cricketNumber of live cricketsMean individual body weight (g)Survival rate
Week 1Week 4Week 1Week 4P-value
Group 160130.0056 ± 0.00070.0247 ± 0.0048g1-g5 = 0.0447

g6-g5 = 0.0213
21.1%
Group 260150.0058 ± 0.00070.0227 ± 0.005225.0%
Group 360110.0057 ± 0.00060.0167 ± 0.005118.3%
Group 460160.0056 ± 0.00080.0158 ± 0.004926.7%
Group 560170.0054 ± 0.00070.0112 ± 0.004628.3%
Group 660120.0058 ± 0.00080.0264 ± 0.005420.0%

Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50–50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

Table 3.

Mean individual body weights and survival rates of individually housed house crickets on week 4

House cricketsNumber of live cricketsMean individual body weight (g)Survival rate
Week 1Week 4Week 1Week 4P-value
Group 1440.0049 ± 0.00490.0136 ± 0.0023g6-g1 = 0.03432

g6-g2 = 0.03933

g6-g3 = 0.01698

g6-g4 = 0.01354

g6-g5 = 0.00558
100%
Group 2440.0050 ± 0.00500.0133 ± 0.0020100%
Group 3440.0052 ± 0.00520.0126 ± 0.0021100%
Group 4440.0052 ± 0.00520.0122 ± 0.0023100%
Group 5440.0049 ± 0.00490.0092 ± 0.0024100%
Group 6440.0050 ± 0.00500.0235 ± 0.0022100%

Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50–50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

Table 3 shows the final BW of the individually housed HCs on week 4 that was significantly higher in Group 6 compared to the other groups. The mean individual BW was the lowest in Group 5 and the highest in Group 6. Significant differences with P-values are shown in Table 3. The survival rate of the individually housed crickets was 100% on week 4.

Tables 4 and 5 show the data on the JFC. There were significant differences in the final BW (P < 0.001) of the group-housed crickets on week 4. The mean individual BW was the lowest in Group 5 and the highest in Group 6. Significant differences with P-values are shown in Table 4. The survival rates of the group-housed JFCs were generally low, with the highest rates in Groups 2 and 4 (28.3%) and the lowest in Group 5 (16.7%), but the differences were not significant (P = 0.36).

Table 4.

Mean individual body weights and survival rates of group-housed Jamaican field crickets on week 4

Jamaican field cricketsNumber of live cricketsMean individual body weight (g)Survival rate
Week 1Week 4Week 1Week 4P-value
Group 160120.0042 ± 0.00040.0238 ± 0.0034g5-g2 = 0.032020.0%
Group 260170.0041 ± 0.00030.0256 ± 0.0038g2-g3 = 0.025428.3%
Group 360150.0041 ± 0.00040.0186 ± 0.0037g2-g4 = 0.043525.0%
Group 460170.0042 ± 0.00040.0192 ± 0.0035g2-g5 = 0.006428.3%
Group 560100.0041 ± 0.00030.0160 ± 0.0037g1-g6 = 0.003616.7%
Group 660120.0042 ± 0.00030.0333 ± 0.0035g2-g6 = 0.016520.0%
g3-g6 < 0.001
g4-g6 < 0.001
g5-g6 < 0.001

Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50–50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

Table 5.

Mean individual body weights and survival rates of individually housed Jamaican field crickets on week 4

Jamaican field cricketNumber of live cricketsMean individual body weight (g)Survival rate
Week 1Week 4Week 1Week 4P-value
Group 1440.0023 ± 0.00070.0150 ± 0.0028100%
Group 2440.0024 ± 0.00050.0141 ± 0.0027g1-g5 = 0.0406100%
Group 3440.0024 ± 0.00060.0120 ± 0.0028g6-g3 = 0.0386100%
Group 4440.0025 ± 0.00070.0112 ± 0.0030g6-g4 = 0.0160100%
Group 5440.0025 ± 0.00050.0079 ± 0.0031g6-g5=<0.001100%
Group 6440.0023 ± 0.00060.0188 ± 0.0029100%

Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50–50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

Table 5 shows the final BW of the individually housed JFCs with significant differences. The mean individual BW was the lowest in Group 5 and the highest in Group 6. Significant differences with P-values are shown in Table 6. The survival rate of individually housed crickets was 100% on week 4.

Table 6.

Mean individual body weights and survival rates of yellow mealworm larvae (YM) on week 14

Yellow mealwormNumber of live mealwormsMean individual body weight (g)Survival rate
Week 1Week 14Week 1Week 14P value
Group 180470.0104 ± 0.00030.0405 ± 0.0044g1-g2 = 0.001258.8%
Group 280550.0105 ± 0.00040.0250 ± 0.0044g1-g3,4,568.8%
Group 380620.0105 ± 0.00040.0188 ± 0.0047<0.00177.5%
Group 480500.0104 ± 0.00030.0183 ± 0.0044g2-g5 = 0.017262.5%
Group 580550.0105 ± 0.00030.0134 ± 0.0044g6-g3 = 0.009468.8%
Group 680150.0105 ± 0.00030.0313 ± 0.0049g6-g4 = 0.006718.8%
g6-g5< 0.001

Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50–50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

The growth tendencies and survival rates of the HCs and the JFCs were similar. The final BW was the highest in Group 6 and the lowest in Group 5. The survival rates were equally poor in both cricket species. However, the survival rate in Group 5 was the highest among the HCs but the lowest among the JFCs. In Group 6, both sexes of HCs and JFCs reached maturity on week 11 and 12, respectively.

Yellow mealworm

The initial and final BW of the YMs were normally distributed with equal variances (P > 0.05). The initial BWs were not significantly different. Table 6 shows the data on the YM larvae. There were significant differences in the final BW (P < 0.001) of the YM larvae on week 14. The mean individual BW was the lowest in Group 5 and the highest in Group 1. Significant differences with P-values are shown in Table 7. Only one individual reached pupation, in Group 1, on week 12.

Table 7.

Substrate reduction of yellow mealworms

Yellow mealwormSubstrate weight (g)
Week 1Week 14Feed consumption
Group 150.17 ± 0.203445.85 ± 0.724.32
Group 250.18 ± 0.213145.56 ± 0.714.73
Group 350.20 ± 0.205444.71 ± 0.665.43
Group 450.18 ± 0.204644.30 ± 0.655.88
Group 550.20 ± 0.211643.41 ± 0.666.79
Group 650.17 ± 0.202746.52 ± 0.713.65

Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50–50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

Table 6 shows the survival rates of the YMs, all above 50%, except for Group 6 that had a very poor survival rate (18.8%). The survival rates were normally distributed with equal variances. Groups 6-1, 2, 3, 4, 5 differed significantly (<0.001).

Table 7 shows the substrate reduction (feed consumption) of the YM groups. The highest substrate reduction was noted in Group 5 and the lowest in Group 6. The substrate reduction differed significantly between Groups 4 and 6 (P = 0.0149) and between Groups 5 and 6 (P = 0.0035).

Table 8 shows the FCR of the YMs. The FCR seemed to gradually worsen with the increase of the urea level. The FCR was the best in Group 6 followed by Group 1 and the worst in Group 5.

Table 8.

Feed conversion ratio of yellow mealworms

Group 1Group 2Group 3Group 4Group 5Group 6
FCR4.16 ± 0.664.43 ± 0.704.88 ± 0.395.73 ± 0.136.65 ± 0.533.49 ± 0.77

FCR: Feed Conversion Ratio, Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50-50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

Superworms

The initial BW of the SWs were normally distributed with equal variances (P > 0.05). Table 9 shows the data on the SWs. The initial BWs were not significantly different. The final BWs were non-normally distributed with equal variances. The mean individual BW was the lowest in Group 5 and the highest in Group 6.

Table 9.

Mean individual body weights and survival rates of superworm larvae on Week 5

Super-wormsNumber of live superwormsMean individual body weight (g)Survival rate
Week 1Week 5Week 1Week 5P-value
Group 160450.0281 ± 0.00140.0449 ± 0.0039g1-g4 = 0.0488

g1-g5 = 0.0202

g2-g5 = 0.0233

g4-g6 = 0.0101

g5-g6 = 0.0029
75.0%
Group 260290.0289 ± 0.00140.0453 ± 0.003348.3%
Group 360340.0285 ± 0.00120.0404 ± 0.003556.7%
Group 460220.0283 ± 0.00110.0352 ± 0.003436.7%
Group 560220.0283 ± 0.00140.0317 ± 0.003336.7%
Group 660200.0281 ± 0.00140.0506 ± 0.003833.3%

Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50–50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

The survival rates were normally distributed with equal variances. The survival rate decreased with the gradual increase of the urea level. The highest was in Group 1 and the lowest was in Group 6. The difference was significant between Group 1-2 (P = 0.0106), 4, 5, 6 (P < 0.001) and Group 3-6 (P = 0.0185).

Table 10 shows the substrate reduction (feed consumption) of the SWs. The feed intake increased with increasing urea inclusion level. The substrate reduction did not differ significantly (P = 0.2076).

Table 10.

Substrate reduction of superworm larvae

SuperwormSubstrate weight (g)
Week 1Week 5Feed difference
Group 150.24 ± 0.2049.58 ± 0.38840.6567
Group 250.19 ± 0.2249.54 ± 0.42200.6545
Group 350.23 ± 0.2049.56 ± 0.42940.6697
Group 450.21 ± 0.2049.2971 ± 0.410.9161
Group 550.23 ± 0.2149.0427 ± 0.381.1907
Group 650.24 ± 0.2249.6283 ± 0.380.6169

Proportions of nitrogen sources in the different groups: Group 1: 100% micellar casein, Group 2: 75% micellar casein, 25% urea; Group 3: 50–50% micellar casein and urea, Group 4: 25% micellar casein, 75% urea, Group 5: 100% urea, Group 6: 100% extracted soybean meal.

The FCR of the SWs seemed to gradually worsen with the increase of the urea level. The FCR was the best in Group 6 followed by Group 1 and the worst in Group 5. Overall, the FCRs were very poor over 15 kg kg−1.

Discussion

Crickets

Several studies showed that the amount, source and quality of protein influence the growth rate of insects. It seems that, in general, poultry diets containing soy are optimal for insects (Sorjonen et al., 2019; Harsányi et al., 2020; Zim et al., 2021). This was also supported by this study as Group 6 (100% extracted soybean meal as a protein source) reached the highest final BW. As previously mentioned, crickets require protein-rich diets (Patton 1978; McCluney and Date, 2008; Lundy and Parrella, 2015; Oonincx et al., 2015; Dobermann et al., 2019; Sorjonen et al., 2019; Morales-Ramos et al., 2020a). Only a few studies tested milk powder or skimmed milk (Patton, 1978; Morales-Ramos et al., 2020a), thus it is difficult to compare the results of this study with those of others. Crickets consuming diets containing skimmed milk developed faster than crickets reared on defatted dry or whole dry milk (Patton, 1978; Morales-Ramos et al., 2020a). The latter study showed a higher consumption of milk powder and of whole milk than of extracted soybean meal. The mean individual BW of group-housed crickets of Group 1 (100% micellar casein) and Group 6 (100% extracted soybean meal) had similar mean individual BWs with crickets kept on chicken feed, while the performance of the other groups was lower (Harsányi et al., 2020). Different harvesting time of insects in other studies makes the comparison of final BWs difficult (Bawa et al., 2020). Higher BW of individually housed crickets in comparison to group-housed individuals was also described by McFarlane (1965). Urea proportions above 25% negatively impacted the final BWs of both group- and individually housed crickets.

The survival rates of group-housed crickets were low. As the proportion of urea did not significantly influence the survival rate, some other reasons must have led to this phenomenon. One reason could be cannibalism, as the survival rates were much better in the individually housed crickets. High mortality was also noted in the study of Oonincx et al. (2015), with survival rates of 6–55% depending on the quality of the feed. The high protein (22.9%) and low fat (1%) diet resulted in the lowest survival rate, while this parameter was the best in the control group (17.2 CP and 4% fat). This might be explained by the presence of cinnamon in the cookie remains which comprised 50% of that diet. On the other hand, Sorjonen et al. (2019) described 80% overall, 94% and 91% survival rates on medium- (22.5%) and high-protein (30.5%) diets in HCs, respectively. In the same study, the overall survival rate of the JFC was 44%, showing better results compared to the ones fed with high-protein (30%) turnip rape and chicken feed (15.2% protein). The proportion of urea did not have a negative impact on the survival rate of crickets. Interestingly, it was the highest (28%) in the 100% urea groups of group-housed crickets. The low survival rate might also be the consequence of a densovirus (AdDNV), which is abundant in European and North American house cricket facilities, interfering with the absorption of nutrients, decreasing growth rates and increasing mortality (Liu et al., 2011; Szelei et al., 2011; Pham et al., 2013; Oonincx et al., 2015).

Crickets reared on chicken feed reached maturity much faster (HC: 34 days and two-spotted cricket [Gryllus bimaculatus]: 24 days) than crickets fed on low-protein barley (45 and 28 days respectively, Sorjonen et al. (2019)). In the study of Oonincx et al. (2015), the development period was between 48 and 167 days depending on the diet. The low protein (12.9%) and high fat (14.6%) diet showed the slowest development time, this paremeter being the highest in the control group (17.2 CP and 4% fat). In the current study, it was difficult to evaluate the development time as only few crickets reached maturity in Group 6 (100% extracted soybean meal). Therefore, the period of 77–84 days was much longer than the results of Sorjonen et al. (2019), but closer to the results of Oonincx et al. (2015).

Mealworms and superworms

Casein supplementation (3 and 20%) increases the BW of YM larvae from 4.08 to 6.16 g (Davis, 1970). In this study, the casein group (Group 1, 100% micellar casein) reached the highest final BW. Likewise, the amino acid composition of milk-derived products seems to be adequate for the YM (Davis and Leclercq, 1969). The proportion of the urea above 25% negatively impacted the final BWs of YMs and SWs. The mean individual BW and weight gain of YMs was lower than that of the larvae kept either on chicken feed or wheat bran (Morales-Ramos and Rojas, 2015; Harsányi et al., 2020). In the study of Oonincx et al. (2015), the determining factor for development was the dietary protein content. Development was faster and survival was better on high-protein diets (22–23%) than on low-protein diets. In the current study, only one individual reached pupation in Group 1 (100% micellar casein) on week 12 which is close to the results of the van Broekhoven study (2015), where it varied between 79 and 168 days. On the other hand, the rest of the mealworms did not reach pupation which requires further investigation. In case of the SW, the isolation prolonged larval development time in comparison to group-housed larvae (Quennedey et al., 1995).

A high protein diet (>21%) improves the survival rate (67%, Oonincx et al., 2015; 80%, van Broekhoven et al., 2015) of the YM, especially if the diet is also rich in carbohydrates. The mortality rate was of >70% during the first 2 months in a study where larvae were reared on either bread or oat flour (Dreassi et al., 2017). The best feed to reach a 50% pupation rate (96.2 ± 3.834 days) was the mixture of beer yeast (5%), wheat flour (47.5%) and oat flour (47.5%). Cannibalism occurs often in mealworm species and has a negative impact on the survival rate (Ichikawa and Kurauchi, 2009). It is difficult to compare the results of this study with those of others, as survival rates were recorded when pupation reached a certain percentage. In the current study, the survival rates were over 50%, but the pupation rate was almost zero. The proportion of urea did not have a negative impact on the survival rate of YMs. Interestingly, it was the second highest (68.8%) in the 100% urea groups. In contrast, the survival rate of SWs was negatively influenced by the increasing urea level which highlights the difference between the two species.

The YM FCRs of the current study were similar to that of Oonincx et al. (2015). It was clear that the FCR of Group 1 (100% micellar casein) and Group 6 (100% extracted soybean meal) were the best, as these feeds were the highest in true protein. FCRs tended to worsen with increasing urea levels, resulting in the worst FCR in Group 5 (100% urea). The SW is not as well studied as the YM, thus the evaluation of FCR results is difficult. Both BW gain and FCR were poor. These findings are in agreement with other studies where feed intake and, consequently, FCR were disadvantageous when larvae were fed with low-quality feeds (Oonincx et al., 2015).

Conclusions

In the HC, the JFC, and the YM on nitrogen basis, urea can replace 25% of micellar casein without having a negative effect on the BW and survival rate, in comparison to the 100% micellar casein group. In the SW, urea supplementation is suggested to be kept below 25%, as higher proportions decreased the survival rate. Further research is needed to find the reasons of high mortality rate of group-housed HCs and SWs, as well as the lack of pupation in YWs.

References

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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
  • 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): Insect mass production technologies. In: Dossey, A.T., Morales-Ramos, J.A., Rojas, M.G. (Eds.), Insects as Sustainable Food Ingredients. Elsevier Academic Press, Amsterdam, the Netherlands, pp. 153201.

    • Search Google Scholar
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    • Search Google Scholar
    • Export Citation
  • Davis, G. R. F. (1975): Essential dietary amino acids for growth of larvae of the yellow mealworm, Tenebrio molitor L. J. Nutr. 105, 10711075.

    • Search Google Scholar
    • Export Citation
  • Davis, G. R. F. and Leclercq, J. (1969): Protein nutrition of “Tenebrio molitor” L. IX. Replacement caseins for the reference diet and a comparison of the nutritional values of various lactalbumins and lactalbumin hydrolysates. Arch. Physiol. Biochem. 77, 687693. https://doi.org/10.3109/13813456909059786.

    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
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    • Search Google Scholar
    • Export Citation
  • Bawa, M., Songsermpong, S., Kaewtapee, C. and Chanput, W. (2020): Effect of diet on the growth performance, feed conversion, and nutrient content of the House cricket. J. Insect Sci. 20, 110. https://doi.org/10.1093/jisesa/ieaa014.

    • Search Google Scholar
    • Export Citation
  • 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): Insect mass production technologies. In: Dossey, A.T., Morales-Ramos, J.A., Rojas, M.G. (Eds.), Insects as Sustainable Food Ingredients. Elsevier Academic Press, Amsterdam, the Netherlands, pp. 153201.

    • Search Google Scholar
    • Export Citation
  • Davis, G. R. F. (1970): Protein nutrition of Tenebrio molitor L. XII. Effects of dietary casein concentration and of dietary cellulose on larvae of race F. Arch. Physiol. Biochem. 78, 3741.

    • Search Google Scholar
    • Export Citation
  • Davis, G. R. F. (1975): Essential dietary amino acids for growth of larvae of the yellow mealworm, Tenebrio molitor L. J. Nutr. 105, 10711075.

    • Search Google Scholar
    • Export Citation
  • Davis, G. R. F. and Leclercq, J. (1969): Protein nutrition of “Tenebrio molitor” L. IX. Replacement caseins for the reference diet and a comparison of the nutritional values of various lactalbumins and lactalbumin hydrolysates. Arch. Physiol. Biochem. 77, 687693. https://doi.org/10.3109/13813456909059786.

    • Search Google Scholar
    • Export Citation
  • Dobermann, D., Michaelson, L. and Field, L. M. (2019): The effect of an initial high-quality feeding regime on the survival of Gryllus bimaculatus (black cricket) on bio-waste. J. Insects Food Feed 5, 117123. https://doi.org/10.3920/JIFF2018.0024.

    • Search Google Scholar
    • Export Citation
  • Dreassi, E., Cito, A., Zanfini, A., Materozzi, L., Botta, M. and Francardi, V. (2017): Dietary fatty acids influence the growth and fatty acid composition of the yellow mealworm Tenebrio molitor (Coleoptera: Tenebrionidae). Lipids 52, 285294. https://doi.org/10.1007/s11745-016-4220-3.

    • Search Google Scholar
    • Export Citation
  • European Parliament and Council (2009): Regulation (EC) No 1069/2009: laying down health rules as regards animal by-products and derived products not intended for human consumption and repealing Regulation (EC) No 1774/2002 (Animal by-products Regulation). Off. J. Eur. Union 300, 133.

    • Search Google Scholar
    • Export Citation
  • Harsányi, E., Juhász, C., Kovács, E., Huzsvai, L., Pintér, R., Fekete, G., Varga, Z. I., Aleksza, L. and Gyuricza, C. (2020): Evaluation of organic wastes as substrates for rearing Zophobas morio, Tenebrio molitor and Acheta domesticus larvae as alternative feed. Insects 11, 604. https://doi.org/10.3390/insects11090604.

    • Search Google Scholar
    • Export Citation
  • Huang, Q., Feng, Y., Shan, H. W., Chen, J. P. and Wu, W. (2023): A novel nitrogen-fixing Bacterium Raoultella electrica isolated from the midgut of the leafhopper Recilia dorsalis. Insects 14:431. https://doi.org/10.3390/insects14050431.

    • Search Google Scholar
    • Export Citation
  • Ichikawa, T. and Kurauchi, T. (2009): Larval cannibalism and pupal defense against cannibalism in two species of tenebrionid beetles. Zoolog. Sci. 26, 525529. https://doi.org/10.2108/zsj.26.525.

    • Search Google Scholar
    • Export Citation
  • Joern, A. and Behmer, S. T. (1997): Importance of dietary nitrogen and carbohydrates to survival, growth, and reproduction in adults of the grasshopper Ageneotettix deorum (Orthoptera: Acrididae). Oecologia 112, 201208. https://doi.org/10.1007/s004420050301.

    • Search Google Scholar
    • Export Citation
  • John, A. M., Davis, G. R. F. and Sosulski, F. W. (1979): Protein nutrition of Tenebrio molitor L. XX. Growth response of larvae to graded levels of amino acids. Arch. Physiol. Biochem. 87, 9971004.

    • Search Google Scholar
    • Export Citation
  • Kröncke, N. and Benning, R. (2022): Self-Selection of feeding substrates by Tenebrio molitor larvae of different ages to determine optimal macronutrient intake and the influence on larval growth and protein content. Insects 13, 657. https://doi.org/10.3390/insects13070657.

    • Search Google Scholar
    • Export Citation
  • Liu, K., Li, Y., Jousset, F-X., Zadori, Z., Szelei, J., Yu, Q., Pham, H. T., Lepine, F., Bergoin, M. and Tijssen, P. (2011): The Acheta domesticus densovirus, isolated from the European house cricket, has evolved an expression strategy unique among parvoviruses. J. Virol. 85, 1006910078. https://doi.org/10.1128/JVI.00625-11.

    • Search Google Scholar
    • Export Citation
  • Lundy, M. E. and Parrella, M. P. (2015): Crickets are not a free lunch: protein capture from scalable organic side-streams via high-density populations of Acheta domesticus. PLoS One 10, 112. https://doi.org/10.1371/journal.pone.0118785.

    • Search Google Scholar
    • Export Citation
  • Makkar, H. P. S., Tran, G., Heuzé, V. and Ankers, P. (2014): State-of-the-art on use of insects as animal feed. Anim. Feed Sci. Technol. 197, 133. https://doi.org/10.1016/j.anifeedsci.2014.07.008.

    • Search Google Scholar
    • Export Citation
  • McCluney, K. E. and Date, R. C. (2008): The effects of hydration on growth of the house cricket, Acheta domesticus. J. Insect Sci. 8, 19. https://doi.org/10.1673/031.008.3201.

    • Search Google Scholar
    • Export Citation
  • McFarlane, J. E. (1965): Studies on group effects in crickets - I. Effect of methyl linolenate, methyl linoleate, and vitamin E. J. Insect Physiol. 12, 179188.

    • Search Google Scholar
    • Export Citation
  • Melis, R., Braca, A., Sanna, R., Spada, S., Mulas, G., Fadda, M. L., Sassu, M. M., Serra, G. and Aneddaet, R. (2019): Metabolic response of yellow mealworm larvae to two alternative rearing substrates. Metabolomics 15, 113. https://doi.org/10.1007/s11306-019-1578-2.

    • Search Google Scholar
    • Export Citation
  • Morales-Ramos, J. A., Rojas, M. G., Shapiro-Llan, D. I., Tedders, W. L. (2013): Use of nutrient self-selection as a diet refining tool in Tenebrio molitor (Coleoptera: Tenebrionidae). J. Entomol. Sci. 48, 206221. https://doi.org/10.18474/0749-8004-48.3.206.

    • Search Google Scholar
    • Export Citation
  • Morales-Ramos, J. A. and Rojas, M. G. (2015): Effect of larval density on food utilization efficiency of Tenebrio molitor (Coleoptera: Tenebrionidae). J. Econ. Entomol. 108, 22592267. https://doi.org/10.1093/jee/tov208.

    • Search Google Scholar
    • Export Citation
  • Morales-Ramos, J. A., Rojas, M. G., Dossey, A. T. and Berhow, M. (2020a): Self-selection of food ingredients and agricultural by-products by the house cricket, Acheta domesticus (Orthoptera: Gryllidae): a holistic approach to develop optimized diets. PLoS One 15, 130. https://doi.org/10.1371/journal.pone.0227400.

    • Search Google Scholar
    • Export Citation
  • Morales-Ramos, J. A., Rojas, M. G., Kelstrup, H. C. and Emery, V. (2020b): Self-selection of agricultural by-products and food ingredients by Tenebrio molitor (Coleoptera: Tenebrionidae) and impact on food utilization and nutrient intake. Insects 11, 115. https://doi.org/10.3390/insects11120827.

    • Search Google Scholar
    • Export Citation
  • Oonincx, D. G. A. B. and de Boer, I. J. M. (2012): Environmental impact of the production of mealworms as a protein source for humans – a life cycle assessment. PLoS One 7, 15. https://doi.org/10.1371/journal.pone.0051145.

    • Search Google Scholar
    • Export Citation
  • 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, 120. https://doi.org/10.1371/journal.pone.0144601.

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  • Orinda, M. A., Mosi, R. O., Ayieko, M. A. and Amimo, F. A. (2017): Growth performance of common house cricket (Acheta domesticus) and field cricket (Gryllus bimaculatus) crickets fed on agro-byproducts. J. Entomol. Zool. Stud. 5, 16641668.

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Senior editors

Editor-in-Chief: Ferenc BASKA

Editorial assistant: Szilvia PÁLINKÁS

 

Editorial Board

  • Mária BENKŐ (Acta Veterinaria Hungarica, Budapest, Hungary)
  • Gábor BODÓ (University of Veterinary Medicine, Budapest, Hungary)
  • Béla DÉNES (University of Veterinary Medicine, Budapest Hungary)
  • Edit ESZTERBAUER (Veterinary Medical Research Institute, Budapest, Hungary)
  • Hedvig FÉBEL (National Agricultural Innovation Centre, Herceghalom, Hungary)
  • László FODOR (University of Veterinary Medicine, Budapest, Hungary)
  • János GÁL (University of Veterinary Medicine, Budapest, Hungary)
  • Balázs HARRACH (Veterinary Medical Research Institute, Budapest, Hungary)
  • Peter MASSÁNYI (Slovak University of Agriculture in Nitra, Nitra, Slovak Republic)
  • Béla NAGY (Veterinary Medical Research Institute, Budapest, Hungary)
  • Tibor NÉMETH (University of Veterinary Medicine, Budapest, Hungary)
  • Zsuzsanna NEOGRÁDY (University of Veterinary Medicine, Budapest, Hungary)
  • Dušan PALIĆ (Ludwig Maximilian University, Munich, Germany)
  • Alessandra PELAGALLI (University of Naples Federico II, Naples, Italy)
  • Kurt PFISTER (Ludwig-Maximilians-University of Munich, Munich, Germany)
  • László SOLTI (University of Veterinary Medicine, Budapest, Hungary)
  • József SZABÓ (University of Veterinary Medicine, Budapest, Hungary)
  • Péter VAJDOVICH (University of Veterinary Medicine, Budapest, Hungary)
  • János VARGA (University of Veterinary Medicine, Budapest, Hungary)
  • Štefan VILČEK (University of Veterinary Medicine in Kosice, Kosice, Slovak Republic)
  • Károly VÖRÖS (University of Veterinary Medicine, Budapest, Hungary)
  • Herbert WEISSENBÖCK (University of Veterinary Medicine, Vienna, Austria)
  • Attila ZSARNOVSZKY (Szent István University, Gödöllő, Hungary)

ACTA VETERINARIA HUNGARICA
Institute for Veterinary Medical Research
Centre for Agricultural Research
Hungarian Academy of Sciences
P.O. Box 18, H-1581 Budapest, Hungary
Phone: (36 1) 287 7073 (ed.-in-chief) or (36 1) 467 4081 (editor)

E-mail: acta.veterinaria@univet.hu (ed.-in-chief)

Indexing and Abstracting Services:

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2022  
Web of Science  
Total Cites
WoS
972
Journal Impact Factor 0.900
Rank by Impact Factor

Veterinary Sciences 95/143

Impact Factor
without
Journal Self Cites
0.900
5 Year
Impact Factor
1.1
Journal Citation Indicator 0.47
Rank by Journal Citation Indicator

Veterinary Sciences 103/170

Scimago  
Scimago
H-index
38
Scimago
Journal Rank
0.277
Scimago Quartile Score

Veterinary (miscellaneous) Q2

Scopus  
Scopus
Cite Score
1.9
Scopus
CIte Score Rank
General Veterinary 76/186 (59th PCTL)
Scopus
SNIP
0.475

2021  
Web of Science  
Total Cites
WoS
1040
Journal Impact Factor 0,959
Rank by Impact Factor Veterinary Sciences 103/144
Impact Factor
without
Journal Self Cites
0,876
5 Year
Impact Factor
1,222
Journal Citation Indicator 0,48
Rank by Journal Citation Indicator Veterinary Sciences 106/168
Scimago  
Scimago
H-index
36
Scimago
Journal Rank
0,313
Scimago Quartile Score Veterinary (miscellaneous) (Q2)
Scopus  
Scopus
Cite Score
1,7
Scopus
CIte Score Rank
General Veterinary 79/183 (Q2)
Scopus
SNIP
0,610

2020  
Total Cites 987
WoS
Journal
Impact Factor
0,955
Rank by Veterinary Sciences 101/146 (Q3)
Impact Factor  
Impact Factor 0,920
without
Journal Self Cites
5 Year 1,164
Impact Factor
Journal  0,57
Citation Indicator  
Rank by Journal  Veterinary Sciences 93/166 (Q3)
Citation Indicator   
Citable 49
Items
Total 49
Articles
Total 0
Reviews
Scimago 33
H-index
Scimago 0,395
Journal Rank
Scimago Veterinary (miscellaneous) Q2
Quartile Score  
Scopus 355/217=1,6
Scite Score  
Scopus General Veterinary 73/183 (Q2)
Scite Score Rank  
Scopus 0,565
SNIP  
Days from  145
submission  
to acceptance  
Days from  150
acceptance  
to publication  
Acceptance 19%
Rate

 

2019  
Total Cites
WoS
798
Impact Factor 0,991
Impact Factor
without
Journal Self Cites
0,897
5 Year
Impact Factor
1,092
Immediacy
Index
0,119
Citable
Items
59
Total
Articles
59
Total
Reviews
0
Cited
Half-Life
9,1
Citing
Half-Life
9,2
Eigenfactor
Score
0,00080
Article Influence
Score
0,253
% Articles
in
Citable Items
100,00
Normalized
Eigenfactor
0,09791
Average
IF
Percentile
42,606
Scimago
H-index
32
Scimago
Journal Rank
0,372
Scopus
Scite Score
335/213=1,6
Scopus
Scite Score Rank
General Veterinary 62/178 (Q2)
Scopus
SNIP
0,634
Acceptance
Rate
18%

 

Acta Veterinaria Hungarica
Publication Model Hybrid
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Acta Veterinaria Hungarica
Language English
Size A4
Year of
Foundation
1951
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 0236-6290 (Print)
ISSN 1588-2705 (Online)

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