Self-selection of food ingredients and agricultural by-products by the house cricket, Acheta domesticus (Orthoptera: Gryllidae): A holistic approach to develop optimized diets


Autoři: Juan A. Morales-Ramos aff001;  M. Guadalupe Rojas aff001;  Aaron T. Dossey aff002;  Mark Berhow aff003
Působiště autorů: USDA-ARS National Biological Control Laboratory, Stoneville, MS, United States of America aff001;  All Things Bugs LLC, Oklahoma City, OK, United States of America aff002;  USDA-ARS National Center for Agricultural Utilization Research, Peoria, IL, United States of America aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227400

Souhrn

The house cricket, Acheta domesticus L. (Orthoptera: Gryllidae) is one of the most important species of industrialized insects in the United States. Within the past five years the market of cricket powder as a food ingredient has been growing with increasing consumer interest on more sustainable sources of food. However, high labor costs of cricket production and high prices of cricket feed formulations result in cricket powder market prices much higher than other protein-rich food ingredients, making cricket powder only competitive within the novelty food market. In this study new diets formulated using by-products were developed using dietary self-selection followed by regression analysis. Crickets selected among seven different combinations of ingredients. Consumption ratios of food ingredients and by-products were used to determine macro and micro-nutrient intake. Regression analysis was used to determine the individual nutrient intake effect on cricket biomass production. Intake of vitamin C, sterol, manganese, and vitamins B1 and B5 had the most significant impact on live biomass production. Four diets were formulated based on this information and compared with a reference (Patton’s 13) and a commercial diet. Although, crickets reared on Patton’s diet 13 produced the most dry-weight biomass and developed the fastest, diet 4 (consisting of 92% by-products) generated the most profit (with a cost of $0.39 USD per kg) after an economic analysis that did not include the commercial formulation. Dry-weight biomass production was not significantly different among the four new diets and the commercial diet. This study demonstrated the value of dietary self-selection studies in developing oligidic insect diets and in studies of insect nutrition. This is the first such study involving farmed edible crickets and agricultural by-products. Four new cricket diet formulations contain between 62 and 92% agricultural by-products are included.

Klíčová slova:

Carbohydrates – Crickets – Diet – Food – Food consumption – Insects – Lipids – Nutrients


Zdroje

1. Dossey AT, Tatum JT and McGill WL. Modern Insect-Based Food Industry: Current Status, Insect Processing Technology, and Recommendations Moving Forward. In: Dossey AT, Morales-Ramos JS, Rojas MG, editors, Insects as Sustainable Food Ingredients: Production, Processing and Food Applications, San Diego (CA): Academic Press; 2016, p. 113–152.

2. Oonincx DGAB, van Itterbeeck J, Heetkamp MJW, van den Brand H, van Loon JJA, van Huis A. An exploration on greenhouse gas and ammonia production by insect species suitable for animal or human consumption. PLoS ONE. 2010; 5(12): e14445. doi: 10.1371/journal.pone.0014445 21206900

3. Gahukar RT. Edible Insects Farming: Efficiency and impact on family livelihood, food security, and environment compared with livestock and crops. In: Dossey AT, Morales-Ramos JS, Rojas MG, editors, Insects as Sustainable Food Ingredients: Production, Processing and Food Applications, San Diego (CA): Academic Press; 2016, p. 85–111.

4. Smetana S, Palanisamy M, Mathys A, Heinz V. Sustainability of insect use for feed and food: Life cycle assessment perspective. J. Cleaner Prod. 2016; 137: 741–751. Internet: http://dx.doi.org/10.1016/j.jclepro.2016.07.148.

5. Steinfeld H, Gerber P, Wassenaar T, Castel V, Rosales M, de Haan C. Livestock’s long shadow. Rome (Italy): Food and Agriculture organization of the United Nations; 2006.

6. Pimentel D, Pimentel M. Sustainability of meat-based and plant-based diets and the environment. Am. J. Clin. Nutr. 2003; 78: 660S–663S. doi: 10.1093/ajcn/78.3.660S 12936963

7. Vogel G. For More Protein, Filet of Cricket. Science. 2010;.327: 811–811. doi: 10.1126/science.327.5967.811 20150488

8. Conway G. One billion hungry: Can we feed the world? Ithaca (NY): Cornell University Press; 2012.

9. Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer TM. Accelerated modern human-induced species losses: Entering the sixth mass extinction. Sci Adv. 2015;1(5): e1400253. doi: 10.1126/sciadv.1400253 26601195

10. Cortes Ortiz JA, Ruiz AT, Morales-Ramos JA, Thomas M, Rojas MG, Tomberlin JK, et al. Insect mass production technologies. In: Dossey AT, Morales-Ramos JS, Rojas MG, editors, Insects as Sustainable Food Ingredients: Production, Processing and Food Applications, San Diego (CA): Academic Press; 2016, p. 153–201.

11. Patton RL. Oligidic diets for Acheta domesticus (Orthoptera: Gryllidae). Ann Entomol Soc Am. 1967; 60: 1238–1242.

12. Nakagaki BJ, DeFoliart GR. Comparison of diets for mass-rearing Acheta domesticus (Orthoptera: Gryllidae) as a novelty food, and comparison of food conversion efficiency with values reported for livestock. J Econ Entomol. 1991; 84: 891–896.

13. van Broekhoven S, Oonincx DGAB, van Huis A, van Loon JJA. Growth performance and feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets composed of organic by-products. J. Ins. Physiol. 2015; 73: 1–10.

14. Nguyen TTX, Tomberlin JK, Vanlaerhoven S. Ability of the black soldier fly (Diptera: Stratiomydae) larvae to recycle food waste. Physiol Ecol. 2015; 44: 406–410.

15. Barragán-Fonseca K, Pineda-Mejia J, Dicke M, van Loon JJA. Performance of the black soldier fly (Diptera: Stratiomydae) on vegetable residue-based diets formulated based on protein and carbohydrate contents. J Econ Entomol. 2018; 111: 2676–2683. doi: 10.1093/jee/toy270 30239768

16. Waldbauer GP, Friedman S. Self-selection of optimal diets by insects. Annu Rev. Entomol. 1991; 36: 43–63.

17. Morales-Ramos JA, Rojas MG, Coudron TA. Artificial diet development for entomophagous arthropods. In: Morales-Ramos JA, Shapiro-Ilan DI, Rojas MD, editors. Mass production of beneficial organisms, invertebrates and entomopathogens. Waltham (MA): Academic Press; 2014. p. 203–240.

18. Cohen AC. Insect diets: Science and technology, second edition. Boca Raton (FL): CRC Press, Taylor & Francis Group; 2015.

19. Waldbauer GP, Cohen RW, Friedman S. Self-selection of an optimal nutrient mix from defined diets by larvae of the corn earworm, Heliothis zea (Boddie). Physiol Zool. 1984; 57: 590–597.

20. Waldbauer GP, Bhattacharya AK. Self-selection of an optimum diet from a mixture of wheat fractions by the larvae of Tribolium confusum. J Ins Physiol. 1973; 19: 407–418.

21. Morales-Ramos JA, Rojas MG, Shapiro-Ilan DI, Tedders DL. Use of nutrient self-selection as a diet refining tool in Tenebrio molitor (Coleoptera: Tenebrionidae). J Entomol Sci. 2013; 48: 206–221.

22. US Department of Agriculture (USDA). USDA national nutrient database for standard reference. Release 28. Beltsville (MD): US Department of Agriculture, Agricultural Research Service, Nutrient Data Laboratory, 2015. http://www.ars.usda.gov/ba/bhnrc/ndl

23. U. S. Grains Council. A guide to distiller’s dried grains with solubles (DDGS). 3rd ed. Washington (DC): U. S. Grains Council; 2012.

24. Blasi DA, Drouillard J, Titgemeyer EC, Paisley SI, Brouk MJ. Soybean hulls. Kansas Agricultural Experiment Station, contribution No. 00-79-E, Manhattan (KS): Kansas State University; 2000.

25. Kahlon TS. Rice bran: production, composition, functionality and food applications, physiological benefits. In: Cho SS, Samuel P, editors. Fiber ingredients: Food applications and health benefits. Boca Raton (FL): CRC Press, Taylor & Francis Group; 2009. p.305–321.

26. Bills CE, Massengale ON, Prickett PS. Factors determining the ergosterol content of yeast: I. Species. J Biol Chem. 1930; 87: 259–264.

27. National Research Council (NRC). United States-Canadian tables of feed composition: Nutritional data for United States and Canadian Feeds. 3rd ed. Washington (DC): National Academy Press; 1982.

28. Wu YV, Stringfellow AC. Corn distillers’ dried grains with solubles and corn distillers’ dried grains: Dry fraction and composition. J food Sci. 1982; 47: 1155–1157 & 1180.

29. Batajoo KK, Shaver KD. In situ dry matter, crude protein, and starch degradabilities of selected grains and by-products. Anim Feed Tech. 1998; 71: 165–176.

30. Spiehs MJ, Whitney MH, Shurson GC. Nutrient database for distiller’s dried grains with solubles produced from new ethanol plants in Minnesota and South Dakota. J Anim Sci. 2002; 80: 2639–2645. doi: 10.2527/2002.80102639x 12413086

31. Huzá S, Várhegyi J, Lehel L, Rózsa L, Kádár M. Mineral content of grains, seeds and industrial by products. Állattenyésztés és Takarmanyozás. 2003; 52: 277–283.

32. Tosch W, Geiger E, Stretz D, Robson GD, Drucker DB. Polar lipids of brewer’s yeast. J Inst Brew. 2005; 111: 197–202.

33. Kim Y, Moiser NS, Hendrickson R, Ezeji T, Blaschek H, Dien B, et al. Composition of corn dry-grain ethanol by-products: DDGS, wet cake, and thin stillage. Bioresource Tech. 2008; 99: 5165–5176.

34. Newkirk R. Canola meal feed industry guide. 4th ed. Winnipeg (Manitoba): Canadian International Grains Institute, Canola Council of Canada; 2009.

35. Jung B, Batal AB, Ward NE, Dale N. Vitamin composition of new-generation corn distillers grains with solubles. J Appl Poult Res. 2013; 22: 71–74.

36. Amorim M, Pereira JO, Gomes D, Pereira CD, Pinheiro H, Pintado M. 2016. Nutritional ingredients from spent brewer’s yeast obtained by hydrolysis and selective membrane filtration integrated in a pilot process. J Food Eng. 2016; 185: 42–47.

37. Morales-Ramos JA, Rojas MG, Dossey AT. Age-dependent food utilization of Acheta domesticus (Orthoptera: Gryllidae) in small groups at two temperatures. J Ins Food Feed. 2018; 4: 51–60.

38. Breslow NE, Clayton DG. Approximate inference in generalized linear mixed models. J. Am. Stat. Assoc. 1993; 88: 9–25.

39. Zar JH. Biostatistical analysis. 4th ed. Upper Saddle River (NJ): Prentice-Hall, Inc.; 1999.

40. Myers RH. Classical and modern regression with applications. Boston (MA): Duxbury Press; 1986.

41. Freund R, Littell R, Creighton L. Regression using JMP®. Cary (NC): SAS Institute Inc.; 2003.

42. SAS Institute. JMP statistical discovery software from SAS, version 12, fitting linear models. Cary (NC): SAS Institute; 2015.

43. Finke MD. Complete nutrient composition of commercially raised invertebrates used as food for insectivores. Zoo Biol. 2002; 21: 269–285.

44. Waldbauer GP. The consumption and utilization of food by insects. Advan Ins Physiol. 1968; 5: 229–288.

45. Nelson PR, Wludyka PS, Copeland AF. The analysis of means: A graphical method for comparing means, rates, and proportions. Philadelphia (PA), Alexandria (VA): ASA-SIAM Series on Statistics and Applied Probability; 2005.

46. AgEBB (Agricultural Electronic Bulletin Board). By-product feed price listening. Columbia (MO): University of Missouri Extension, College of Agriculture, Food and Natural Resources; 2019. http://agebb.missouri.edu/dairy/byprod/listing.php

47. Alibaba.com. Agriculture and food. 2019. https://www.alibaba.com/Products?spm=a2700.8293689.scGlobalHomeHeader.341.105b65aaLQc0ko

48. USDA. Food markets & prices. U. S. Department of Agriculture, Economic Research Service; 2019b. https://www.ers.usda.gov/topics/food-markets-prices/

49. Lundy ME, Parrella MP. Crickets are not a free lunch: protein capture from scalable organic side-streams via high-density populations of Acheta domesticus. PLoS ONE. 2015; 10(4): e0118785. doi: 10.1371/journal.pone.0118785 25875026

50. Schiff NM, Waldbauer GP, Friedman S. Dietary self-selection for vitamins and lipid by larvae of the corn earworm, Heliothis zea. Entomol. Exp. Appl. 1988; 42: 240–256.

51. Trumper S, Simpson SJ. Regulation of salt intake by nymphs of Locusta migratoria. J. Ins. Physiol. 1993; 39: 857–864.

52. Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D. Optimal foraging when regulating intake of multiple nutrients. Anim. Behav. 2004; 68: 1299–1311.

53. House HL. Insect nutrition. Annu. Rev. Entomol. 1961; 6: 13–26.

54. Downer RG. Functional role of lipids in insects. In: Rockstein M, editor. Biochemistry of Insects. New York (NY): Academic Press; 1978. pp. 57–92

55. McFarlane JE. Nutrition and digestive organs. In: Blum MS, editor. Fundamentals of Insect Physiology. New York (NY): John Wiley and Sons; 1985. pp. 59–89.

56. Chapman RF. The insects, 4th edition. Cambridge, UK: Cambridge University Press; 1998.

57. Neville PF, Stoone PC, Luckey TD. Cricket nutrition II. An unidentified factor in the nutrition of Acheta domesticus. J. Nutr. 1961; 74: 265–273.

58. Finke MD. Complete nutrient content of four species of commercially available feeder insects fed enhanced diets during growth. Zoo Biol. 2015; 34: 554–564. doi: 10.1002/zoo.21246 26366856

59. Ulrich RG, Buthala DA, Klug MJ. Microbiota associated with the gastrointestinal trac of the common house cricket, Acheta domesticus. Appl. Environ. Microbiol. 1981; 41: 246–254. 16345692

60. Kaufman MG, Klug MJ, Merritt RW. Growth and food utilization parameters of germ-free house crickets, Acheta domesticus. J. Ins. Physiol. 1989; 35: 957–967.

61. Keuth S, Bisping B. Formation of vitamins by pure cultures of tempe molds and bacteria during tempe solid substrate fermentation. J. Appl. Bacteriol. 1993; 75: 427–434. doi: 10.1111/j.1365-2672.1993.tb02798.x 8300444

62. Huynh MP, Hibbard BE, Lapointe SL, Niedz RP, French BW, Pereira AE, et al. Multidimensional approach to formulating a specialized diet for northern corn rootworm larvae. Scientific reports. 2019; 9: 3709. doi: 10.1038/s41598-019-39709-x 30842452

63. Lapointe SL, Evens TJ, Niedz RP. Insect diets as mixtures: optimization for a polyphagous weevil. J. ins. Physiol. 2008; 54: 1157–1167.

64. Pascacio-Villafán C, Birke A, Williams T, Aluja M. Modeling the costeffectiveness of insect rearing on artificial diets: A test with a tephritid fly used in the sterile insect technique. PloS one. 2017; 12(3), e0173205. doi: 10.1371/journal.pone.0173205 28257496

65. Raubenheimer D. Towards a quantitative nutritional ecology: the right-angled mixture triangle. Ecol. Monogr. 2011; 81: 407–427.


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