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Effects of powderization of a granular diet on growth performance of the edible cricket, Teleogryllus occipitalis (Orthoptera: Gryllidae)

In: Journal of Insects as Food and Feed
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K. Murata Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Nakacho 2-24-16, Koganei, Tokyo 184-8588, Japan

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W. Kagesawa Department of Nutrition and Food Science, Ochanomizu University, Otsuka 2-1-1, Bunkyo, Tokyo 112-8610, Japan

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M. Akechi Department of Nutrition and Food Science, Ochanomizu University, Otsuka 2-1-1, Bunkyo, Tokyo 112-8610, Japan

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Y. Morimitsu Department of Nutrition and Food Science, Ochanomizu University, Otsuka 2-1-1, Bunkyo, Tokyo 112-8610, Japan

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T. Suzuki Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Nakacho 2-24-16, Koganei, Tokyo 184-8588, Japan

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Open Access

Abstract

Farming edible crickets has environmental and nutritional benefits, as well as social benefits such as livelihood diversification. Commercial feeds for poultry and fish farming are often used to feed crickets, and in recent years, crop and food-processing by-products have also been used to improve sustainability. However, the design of feed for crickets has not been standardized. Here, we investigated growth and development of the Asian field cricket, Teleogryllus occipitalis (Audinet-Serville) (Orthoptera: Gryllidae), fed on different forms of the same diet. Body mass and the rate of development were significantly greater in crickets fed on millimetre-order granules than in crickets fed on micrometre-order powder. In addition, analysis of feeding behaviour revealed that crickets fed less frequently on the powdered diet than on the granulated diet. These results suggest that crickets have an avoidance behaviour towards fine particles, or that the granular form is easier for them to grasp and ingest than the powdery form, which may have contributed to growth performance. Simply feeding millimetre-order granules may contribute to the development of feed design for farming edible crickets.

1 Introduction

Edible-insect farming has attracted worldwide attention as an environmentally friendly source of animal protein and micronutrients (van Huis et al., 2013). Crickets are one of the most suitable insect groups for farming because of their rapid development, high fecundity, omnivorous nature, and ability to grow on dry feed as long as they are watered (Simmons, 2005; Gutiérrez et al., 2020). In addition, the feed conversion ratio of crickets is 5.9 times that of beef cattle (van Huis, 2013), and the amount of greenhouse gases emitted by cricket farming is about one-quarter (CO2 + CO2-eq.) of that emitted by beef cattle farming (Oonincx et al., 2010). The use of crickets as a food source is growing. In Thailand, approximately 20,000 farmers produce crickets, and annual production averaged about 7,500 t from 1996 to 2011 (Hanboonsong et al., 2013). The European house cricket, Acheta domesticus (L.) (Orthoptera: Gryllidae), is the third insect species to be authorized as a novel food by the European Commission (2022).

Commercial feed for poultry and fish farming has often been used as cricket feed (Hanboonsong et al., 2013; Miech et al., 2016). In poultry farming, it is well known that the aggregate size of feed affects growth performance. For example, the body mass of broilers fed a diet in crumb or pellet form tends to be higher than that of those fed mash, which is in powdered form (Reece et al., 1985; Svihus et al., 2004). Naser El Deen et al. (2022) reported that larvae of the mealworm, Tenebrio molitor L. (Coleoptera: Tenebrionidae), showed greater growth when fed on a diet with a particle size less than 2 mm. Patton (1967) described that A. domesticus nymphs tended to prefer smaller diet to larger one, but they presented no objective data such as size. No other studies have reported the effect of diet size on the performance of crickets.

Here, we show that diet size on its own affects developmental time and adult body mass of the Asian field cricket, Teleogryllus occipitalis (Audinet-Serville) (Orthoptera: Gryllidae), a traditional food species in East and South-East Asia.

2 Materials and methods

2.1 Insects

We used a population of Tel. occipitalis collected on Amami Ohshima (Kagoshima, Japan) and previously used for whole-genome sequencing (Kataoka et al., 2020). This population was maintained on chicken feed (Chougenki Edzukeyousuuyou; Nosan Corp., Yokohama, Japan) or goldfish feed (Kingyo Genki Probio Flake; GEX Corp., Osaka, Japan) and water in polypropylene containers at 25 °C with uncontrolled relative humidity (RH).

2.2 Diet processing and aggregate size distribution

We bought an experimental diet for insects (I; Oriental Yeast Co., Ltd., Tokyo, Japan) in granular form. The main nutrition components measured are listed in Supplementary Table S1. The powdered form was prepared from it in a food processor (SG-10BKJ; Conair Japan G. K., Tokyo, Japan). We took images of the granular diet with an image scanner (GT-X980; Seiko Epson Corp., Tokyo, Japan) and of the powdered diet with a scanning electron microscope (TM-3030; Hitachi High-Tech Corp., Tokyo, Japan). We used the images to calculate the aggregate size distribution by using the ROI manager and selection brush tool of NIH ImageJ 1.53 k software (Schneider et al., 2012) to measure the area (S) and calculating the aggregate size as that of a circle with the same diameter (Φ), as:
(1) Φ = 2 S π

2.3 Growth performance assay

A polypropylene container (239 mm × 176 mm × 91 mm) with a lid perforated with ∼100 holes (2.5 mm in diameter) for ventilation was used as a rearing container for each treatment. Non-woven fabric (Nougyouyoufushokufu; MonotaRO Co., Ltd., Osaka, Japan) was placed between the container and the lid to prevent escape of young nymphs. A polystyrene cup (V-9; As One Corp., Osaka, Japan) filled with water was prepared in the rearing container. A single hole (10 mm in diameter) was made in its lid, and a paper towel (Crecia EF Hand Towel Soft Type; Nippon Paper Crecia Co., Ltd., Tokyo, Japan) was placed through the hole and touching the water to provide a watering station. Two pieces (10 cm × 15 cm) of cardboard egg carton were put into each container as shelter to mitigate cannibalism. The diet was put into a polystyrene Petri dish (90 mm diameter) placed on the egg cartons and replenished as needed to prevent depletion. Kimtowels (Nippon Paper Crecia Co., Ltd.) were placed in each container to facilitate access for the crickets to the watering station and feeding area.

Wet cotton on which cricket eggs were laid was collected from the stock population and placed in the polystyrene cup. The cup was covered with a non-perforated lid and maintained in an incubator (MIR-554-PJ; PHC Holdings Corp., Tokyo, Japan) at 30 °C with uncontrolled RH (but the inside of the cup would be at saturated water vapor pressure) until hatching. First-instar nymphs hatched within 24 h were collected and allocated among the containers (50 in each) on day 0, and reared under a 16-h light and 8-h dark cycle (LD 16:8) at 30 °C with uncontrolled RH. The number of individuals in each container was recorded on days 6, 13, 20, 27, 34 and 41. Fresh body mass of 10 nymphs randomly collected from each container was individually measured on an electronic balance (FX-500i; A&D Co., Ltd., Tokyo, Japan) on days 20, 27, 34 and 41. When adults emerged, we calculated the developmental day and measured the fresh body mass on the electronic balance and the head width, pronotum length, pronotum width, forewing length and hind-leg femur length with a digital calliper (CD67-S15PS; Mitsutoyo Corp., Kawasaki, Japan). Adults were removed from each container after measurement and the bioassay was continued until all surviving crickets had reached the adult stage. The bioassay consisted of three independent experimental runs.

2.4 Calculation of population growth rate

To evaluate the daily yield, we calculated the population growth rate (PGR, g day−1) as:
(2) PGR = k = 1 n m k T k
where k = number of crickets tested, n = number of adults emerged, T k = developmental days from hatching to adult emergence of each individual, and m k = fresh body mass (g) of each adult within 24 h after emergence.

2.5 Morphological analyses of mouthparts

First-instar nymphs and adults were anaesthetised, decapitated, mounted on holders using double-sided carbon tape, and the mouthparts of non-treated samples were observed through a scanning electron microscope (VHX-DF510; Keyence Corp., Osaka, Japan) at 1.2 kV acceleration voltage. From the images, widths of the labrum were calculated from the images as an approximation of the mandibular range.

2.6 Feeding behaviour assay

The feeding behaviour of eight cricket nymphs weighing 0.18 ± 0.01 g (mean ± SE) was recorded to compare preference between the granular (n = 4) and powdered (n = 4) diets. The recording system was adapted from Hayakawa et al. (2024). The nymphs were individually placed in a transparent acrylic box (137 mm × 65 mm × 37 mm) containing a polystyrene Petri dish (35 mm diameter) filled with 1.5 g of the granular or powdered diet, and a wet hemp string as a watering device, one end of which penetrated the wall of the each box and the other end of which was connected to a water tank (V-3; As One Corp.) located outside of the each box. To make the individuals invisible to each other, cardboard walls (50 mm high) were placed between each box. After a 24-h acclimation period for the nymphs in the box, time-lapse photography was performed using an infrared camera module 3 (Raspberry Pi NoIR Wide; 4,608 × 2,592 pixels) connected to a Raspberry Pi 3 model B (Raspberry Pi Foundation, Cambridge, UK), which captured RGB images of the crickets at 1-min intervals for 24 h. During this period, diets and water were not replenished or replaced. The camera was positioned 350 mm above the bottom of the acrylic boxes. The experimental system was installed in an incubator (MIR-253; Sanyo Electric Co., Ltd., Osaka, Japan) at 30 °C with uncontrolled RH. Illumination was provided by white LEDs (Timely, Tokyo, Japan) and infrared LEDs (Broadwatch, Tokyo, Japan). The white LEDs were connected to a time switch to ensure the LD 16:8 cycle. From the time-lapse images, the frequency of the nymphal head located on the diet dish was counted to estimate the feeding frequency.

2.7 Statistical analyses

All data analyses and visualizations were performed in R v. 4.4.1 software. Statistical differences between the means of growth performance and feeding behaviour data were analysed with Student’s t-test, Welch’s t-test, the Wilcoxon–Mann–Whitney U-test, or the Brunner–Munzel test, according to the data distribution and variance. Statistical differences of the Kaplan–Meier survival curves were analysed by log-rank test. A statistical difference between two categorical variables, such as adult emergence, was analysed with Fisher’s exact test. Pearson’s or Spearman’s rank correlation coefficient tests were performed for all correlation analyses according to the data distribution.

3 Results

3.1 Aggregate size distribution

Aggregate sizes (median [first quartile, third quartile]) were 2.287 mm [2.593 mm, 2.800 mm] in the granular diet (n = 170) and 25.74 μm [16.20 μm, 39.83 μm] in the powdered diet (n = 327) (Figure 1). The size distributions did not overlap.

Figure 1
Figure 1

Images of (A) granular diet taken with an image scanner and (B) powdered diet taken by SEM, and aggregate size distributions of (C) granular and (D) powdered diet. Numerical values for the aggregate size are presented as medians (first quartile, third quartile).

Citation: Journal of Insects as Food and Feed 2024; 10.1163/23524588-00001255

Figure 2
Figure 2

Growth performance of Teleogryllus occipitalis reared on a granular or a powdered diet. (A) Fresh body mass of nymphs at 20, 27, 34 and 41 days after hatching (Wilcoxon–Mann–Whitney U-test for Days 20 and 27; Welch’s t-test for Days 34 and 41). (B) Survival curves of nymphs (log-rank test). (C) Rates of adult emergence from nymphs (Fisher’s exact test). Values are means ± SE of three independent experimental runs. (D) Developmental time of crickets (Wilcoxon–Mann–Whitney U-test). (E) Fresh body mass of adult crickets (Welch’s t-test). (F) Population growth rate (PGR) of crickets (Student’s t-test). Values are means ± SE of three independent experimental runs. The initial number of crickets tested was 50 in each experimental run. Green circles and black crosses indicate individual data from three independent experimental runs and the mean of each run, respectively.

Citation: Journal of Insects as Food and Feed 2024; 10.1163/23524588-00001255

Figure 3
Figure 3

Body part dimensions in Teleogryllus occipitalis adults fed on a granular or a powdered diet. (A) Head width (Brunner–Munzel test). (B) Pronotum length (Welch’s t-test). (C) Pronotum width (Brunner–Munzel test). (D) Forewing length (Welch’s t-test). (E) Hind-leg femur length (Brunner–Munzel test). Green circles and black crosses indicate individual data from three independent experimental runs and the mean of each run, respectively.

Citation: Journal of Insects as Food and Feed 2024; 10.1163/23524588-00001255

Figure 4
Figure 4

Correlations of fresh mass of adult body with (A) head width, (B) pronotum length, (C) pronotum width, (D) forewing length, (E) hind-leg femur length and (F) developmental time in Teleogryllus occipitalis fed on ∙ granular or ∘ powdered diet. Spearman’s rank correlation coefficient tests were performed for all correlation evaluations.

Citation: Journal of Insects as Food and Feed 2024; 10.1163/23524588-00001255

3.2 Growth performance of crickets

Fresh body mass of nymphs reared on the granular diet was significantly higher than those of nymphs reared on the powdered diet at 20, 27, 34 and 41 days after hatching ( P < 0.05; Figure 2A). There was no significant difference in the survival curves between diets ( P > 0.05; Figure 2B). The rate of adult emergence from nymphs fed on the granular diet was 66 ± 9 % (mean ± SE) – significantly higher than that from nymphs fed on the powdered diet (39 ± 7 %, P < 0.001; Figure 2C). The developmental time of crickets fed on the granular diet was 53 ± 1 days (mean ± SE) – significantly shorter than that of crickets fed on the powdered diet (62 ± 1 days, P < 0.001; Figure 2D). The adult body mass of crickets fed on the granular diet was 0.53 ± 0.01 g (mean ± SE) – significantly heavier than that of crickets fed on the powdered diet (0.38 ± 0.01 g, P < 0.001; Figure 2E). PGR tended to be greater in crickets fed on the granular diet ( P = 0.09; Figure 2F). Head width, pronotum length, pronotum width, forewing length and hind-leg femur length of crickets fed on the granular diet were significantly larger than those of crickets fed on powdered diet ( P < 0.001; Figure 3). In all adult crickets, adult body mass was correlated positively with the size of each body part ( P < 0.001, r > 0.8, Figure 4A–4E) and negatively with developmental time ( P < 0.001, r = 0.68, Figure 4F). The similar trends were also observed even when the data of each treatment were analysed separately (Supplementary Tables S2 and S3).

3.3 Distance between mandibles of nymphal and adult crickets

The labrum width (mean ± SE) as an approximation of the distance between the mandibles (Figure 5A-D) was 0.223 ± 0.002 mm (n = 9) in first-instar nymphs and 1.853 ± 0.023 mm (n = 9) in adults. As the mandibles of crickets are often covered by the labrum when closed, it is difficult to measure their range. However, as the mandibles open during CO2 anaesthesia (personal observation), to assess the validity of labrum width as an approximation of the mandibular range, labrum width and the range of forced-open mandibles were measured in nymphs and adults (n = 9), which were different individuals from those mentioned above. The range of forced-open mandibles by CO2 anaesthesia showed a trend towards a positive correlation with the labrum width ( r = 0.62, P = 0.075; Figure 5E), although the degree of opening varied.

Figure 5
Figure 5

Head images of (A, C) a first-instar nymph and (B, D) an adult of Teleogryllus occipitalis with mandibles (A, B) opened and (C, D) closed. ↔ Labrum width (LW) and mandibular range (MR). (E) The relationship between LW and MR when the mandibles of nymphs and adults were forced open under CO2 anaesthesia (n = 9).

Citation: Journal of Insects as Food and Feed 2024; 10.1163/23524588-00001255

3.4 Preference of dietary form

Nymphal feeding frequencies (mean ± SE) on the granular and powdered diets, measured at a resolution of 1 min for 24 h, were 268.3 ± 33.4 (n = 4) and 24.3 ± 7.7 (n = 4), respectively, and there was a significant difference between them ( P = 0.004; Figure 6).

4 Discussion

As far as we know, ours is the first study to demonstrate that diet size affects the growth performance of crickets. Most of the growth parameters of Tel. occipitalis fed a millimetre-order granular diet were superior to those fed a micrometre-order powdered diet, even though the nutrient composition of the diets was identical.

Although the survival of crickets from hatching to first adult emergence (41 days after hatching) did not differ between the two diets, the body mass of nymphs and adults fed on the granular diet was higher than those of crickets fed on the powdered diet (Figure 2). However, because the body mass of insects often varies greatly depending on the timing of feeding and the water intake, the head width, pronotum length, pronotum width, forewing length and hind-leg femur length are often used as more accurate growth parameters of orthopteran insects (Arai and Watanabe, 2019). The lengths of all five of these body parts were significantly greater in adults that emerged from nymphs fed on the granular diet (Figure 3), and they had significant positive correlations with the adult body mass (Figure 4A-E); thus, body mass is also an accurate growth parameter, at least in Tel. occipitalis adults within a day after emergence. In contrast, adult body mass had a significant negative correlation with developmental time (Figure 4F). This result is not consistent with Masaki (1978) that head width and developmental time were positively correlated in the lawn ground cricket, Polionemobius taprobanensis (Walker) (Orthoptera: Trigonidiidae). In addition, there was no correlation between adult body mass and developmental time in Tel. occipitalis fed on chicken feed (unpublished data). The correlation between developmental time and adult body mass of crickets may vary with nutritional conditions during the nymphal period. Further studies are needed to investigate this hypothesis.

The feeding frequency, estimated from the position of the nymphal head that could access the diet, was significantly higher for the granular diet than for the powdered diet (Figure 6). The low frequency of nymphal access to the powdered diet (Figure 6B) suggests their avoidance of fine particles rather than the attractiveness of granular forms to them. The German cockroach, Blattella germanica (L.) (Blattodea: Blattellidae), is known to groom itself to remove dust from its body surface (El-Awami and Dent, 1995). In the field cricket, Tel. oceanicus (Le Guillou) (Orthoptera: Gryllidae), grooming is thought to be important for maintaining the working condition of the sensory apparatus (Lefebvre, 1981). Thus, at least for insects that exhibit grooming behaviour, fine particles adhering to the body are an object to be avoided, and this may be the reason why the frequency of feeding on powdered diet was lower than that on granulated diet.

Figure 6
Figure 6

Feeding behaviour of Teleogryllus occipitalis nymphs on granular or powdered diet under an LD 16:8 cycle at 30 °C for 24 h. (A) The frequency of feeding at a resolution of 1 min for 24 h (Welch’s t-test). (B) The time-course of feeding behaviour. The black vertical lines form a stacked bar chart of the number of feedings every eight minutes. The black and white horizontal bars at the top of each graph indicate the dark and light periods, respectively.

Citation: Journal of Insects as Food and Feed 2024; 10.1163/23524588-00001255

Mantids – predatory polyneopteran insects – grasp their prey in their forelegs. The preferred prey size of the mantid, Hierodula crassa Giglio-Tos (Mantodea: Mantidae), is predictive of the lengths of the femur and tibia of the foreleg and the angle between them (Holling, 1964). Crickets, which are also polyneopteran insects, grasp their food mainly in their mandibles (Winkler et al., 2024). The width of labrum for estimating the mandibular range in Tel. occipitalis was 0.223 mm in first-instar nymphs and 1.853 mm in adults (Figure 5). Therefore, crickets that ingested granular diet (2.56 ± 0.03 mm; Figure 1) larger than their mandibular range first had to gnaw it down to a suitable size. In contrast, the powdered diet, with a smaller size (25.74 μm; Figure 1), was less suitable for grasping in the crickets’ mandibles. Initially, we hypothesized that the powdered diet with smaller aggregate sizes was difficult for crickets to grasp with their mandibles, resulting in reduced feeding compared to the granular diet and thus inhibiting their growth and development. However, if this is true, it would be reasonable to expect that crickets would increase their feeding frequency in order to obtain nutrients from the powder diet, which is potentially hard to grasp with their mandibles. In fact, however, the frequency of feeding on the powdered diet was clearly lower than that on the granular diet (Figure 6), suggesting that in the present study, avoidance behavior of crickets toward fine particles, rather than ease of grasping with their mandible, affected their growth and development.

5 Conclusion

The growth and development of Tel. occipitalis reared on a granular diet were significantly superior to those of Tel. occipitalis reared on a powdered but otherwise identical diet. This difference may be primarily due to the reduced frequency of feeding on the powdered diet, indicating crickets may exhibit avoidance behavior toward fine particles. In addition, a size that crickets’ mandibles can grasp could affect their ingestion. We plan to investigate these potential effects in order to optimize the form of diet in the production of edible crickets.

*

Corresponding author; e-mail: tszk@cc.tuat.ac.jp

Supplementary material

Supplementary material is available online at: https://doi.org/10.6084/m9.figshare.26983534

Acknowledgements

We thank Dr Masanobu Yamamoto, Mr Takuma Takahashi, and Dr Wuled Lenggoro of the Tokyo University of Agriculture and Technology (TUAT) for useful discussions and for sharing knowledge of particle suspensions in water. We also thank Dr Susumu Inasawa of TUAT for his guidance in the use of the scanning electron microscope. This work was supported partly by the Cabinet Office, Government of Japan Cross-ministerial Moonshot Agriculture, Forestry and Fisheries Research and Development Program, “Technologies for Smart Bio-industry and Agriculture” (funded by the Bio-oriented Technology Research Advancement Institution) (JPJ009237).

Conflict of interest

The authors have no conflict of interest to declare.

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