PLANT BIOLOGY
ANIMAL BIOLOGY
SUBSCRIPTION
E-SUBSCRIPTION
 
MAP
MAIN PAGE

 

 

 

 

Mechtaeva E.V., Zerov A.V., Dzyubenko V.V., Sorokoumov P.N., Novikova M.V., Ryabukhin D.S., Zhuravleva A.Z., Sitnov V.Yu. Influence of antibiotic ceftriaxone on the developmentof the yellow mealworm beetle (Tenebrio molitor L.). Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2024, Vol. 59, № 3, p. 571-581.
(how to cite this article)

doi: 10.15389/agrobiology.2024.3.571eng

UDC: 638.45:636.087

Acknowledgements:
This research was part of the research topics № FGUS-2024-0010 and № FGUS-2022-0018.

 

INFLUENCE OF ANTIBIOTIC CEFTRIAXONE ON THE DEVELOPMENT OF THE YELLOW MEALWORM BEETLE (Tenebrio molitor L.)

E.V. Mechtaeva ✉, A.V. Zerov, V.V. Dzyubenko, P.N. Sorokoumov,
M.V. Novikova, D.S. Ryabukhin, A.Z. Zhuravleva, V.Yu. Sitnov

All-Russian Research Institute for Food Additives — Branch of Gorbatov Federal Research Center for Food Systems RAS, 55, Liteyny prospekt, St. Petersburg, 190000 Russia, e-mail mechtaeva.lisa@gmail.com (✉ corresponding author),  zzerovaleksei1995@gmail.com, torrid18@yandex.ru, sorokoumov_pavel@mail.ru, mariazakharova@bk.ru,
rdms@bk.ru, aigul-zhuravleva@mail.ru, v.sitnov@fncps.ru

ORCID:
Mechtaeva E.V. orcid.org/0000-0001-7879-7994
Novikova M.V. orcid.org/0000-0002-4195-0649
Zerov A.V. orcid.org/0000-0003-4296-5225
Ryabukhin D.S. orcid.org/0000-0001-5345-0038
Dzyubenko V.V. orcid.org/0000-0002-8145-122X
Zhuravleva A.Z. orcid.org/0009-0003-2683-269X
Sorokoumov P.N. orcid.org/0000-0002-8767-3720
Sitnov V.Yu. orcid.org/0000-0003-1927-1997

Final revision received October 23, 2023
Accepted November 13, 2023

Antibiotics can enter the soil with waste and affect insects in their natural habitat, moreover they are often found in feed for farm animals, which is also used for rearing insects for food and feed. In addition, the possibility of bioconversion of agricultural waste with larvae is currently being widely studied. Such waste may contain significant amounts of antibiotics, which affect the growth, development and microbiota of insects used to process it. Ceftriaxone is a third-generation cephalosporin antibiotic. The influence of cephalosporin antibiotics on insects is little studied, while it depends on both the insect species and the type of antibiotic. The yellow mealworm beetle is an ediable insect and a pest of grain products, most often found in the bins of flour warehouses, bakeries, mills, and feed. In this work, the effect of different concentrations of the ceftriaxone on the weight and survival rate of the T. molitor larvae, several parameters of larvae composition, as well as metamorphosis and the number of offspring was shown. The ability of T. molitor to consume the feed substrate or process waste containing ceftriaxone was demonstrated for the first time. The aim of this work was to study the effect of the antibiotic ceftriaxone on the growth, development and reproductive performance of the yellow mealworm. The experiments were carried out in the insectarium of the All-Russian Research Institute for Food Additives (St. Petersburg, Russia) from July to October 2022. Before the experiment, the insects were reared at 25±2 °C and relative humidity of 50±10 %. A diet for yellow mealworm were composed of wheat bran (16.0 g proteins, 4.0 g fats, 65,0 g carbohydrates per 100 g of the product) and carrot as a source of water. The effect of ceftriaxone (Biosintez, Russia) on insects at concentrations of 0, 0.1, 1, 10, and 100 mg/kg of feed (wheat bran) dry weight was studied. To obtain the feed with certain antibiotic concentration the following procedure was carried out: ceftriaxone solutions with required concentration were added to wheat bran in a 1:1 ratio and thoroughly mixed, then the feed was dried in a convection dryer UF110plus (Memmert GmbH & Co.KG, Germany) at 40 °C for 24 h. The experiment included three stages: the study of the growth rate of larvae, the calculation of the number of pupated and turned into adult insects, and the assessment of the number of T. molitor offspring. Feed conversion ratio (FCR) and efficiency of conversion of digested food (ECD) were calculated. FCR and ECD were calculated given wet feed (bran + carrots) and for bran weight only. The water content of the larvae was determined by drying a sample in the Vacuum Oven OV-12 (Jeio Tech, Korea) at 40 °C. To determine the ash content of the larvae, dried samples were placed in crucibles calcined to constant weight and burned in a SNOL 8.2/1100 muffle furnace (Umega Group, AB, Lithuania) using the following calcination regime: 60 min at 250 °C + 6 h at 550 °C. The fatty acid composition was determined by gas chromatography with mass spectrometry detection on a gas chromatograph Varian 450-GC GC (Varian Chromatography Systems, Netherlands) with a mass spectrometer detector Varian 240-MS (Varian, Inc., USA). Methylation and extraction of fatty acids from samples dried in the Vacuum Oven OV-12 at 40 °C was carried out using a 15 % solution of sulfuric acid in methanol and chloroform. The results of the study showed that the addition of ceftriaxone to the diet of the yellow mealworm beetles at a concentration of 100 mg/kg led to the acceleration in weight gain by the larvae (p = 0.029). No relationship was observed between T. molitor larval survival rate and antibiotic concentration (p > 0.05). In addition, no statistically significant differences were found between the fatty acid composition, feed conversion ratios, ash content and water content of the larvae fed on wheat bran with different ceftriaxone concentrations (p > 0.05). There was no relationship between the antibiotic content (0-100 mg/kg) and the productivity of the yellow mealworm, and no changes were found in the processes of pupation and transformation into imago when the antibiotic was added to the feed (p > 0.05). Therefore, T. molitor can be reared on a diet containing ceftriaxone while maintaining the vitality and basic characteristics of insects necessary for their further use. In addition, these results mean that ceftriaxone does not adversely affect the large mealworm beetles as a pest of grain crop products.

Keywords: Tenebrio molitor, yellow mealworm, antibiotics, ceftriaxone, larvae, imago, adults, oviposition.

 

REFERENCES

  1. Lakew A., Megersa N., Chandravanshi B.S. Trace level enrichment and clean-up of β-lactam antibiotic residues in edible chicken tissues and feathers by solid phase extraction for quantitative determination utilizing liquid chromatography. Bulletin of the Chemical Society of Ethiopia, 2022, 36(3): 503-519 CrossRef
  2. Ismail M.M. Pharmacokinetics, urinary and mammary excretion of ceftriaxone in lactating goats. Journal of Veterinary Medicine Series A, 2005, 52(7): 354-358 CrossRef
  3. Levy S.B. Emergence of antibiotic-resistant bacteria in the intestinal flora of farm inhabitants. The Journal of Infectious Diseases, 1978, 137(5): 688-690.
  4. Kim K.-R., Owens G., Kwon S.-I., So K.-H., Lee D.-B., Ok Y.S. Occurrence and environmental fate of veterinary antibiotics in the terrestrial environment. Water, Air, & Soil Pollution, 2011, 214: 163-174 CrossRef
  5. De Liguoro M., Cibin V., Capolongo F., Halling-Sørensen B., Montesissa C. Use of oxytetracycline and tylosin in intensive calf farming: evaluation of transfer to manure and soil. Chemosphere, 2003,52(1): 203-212 CrossRef
  6. Li T., Zhang Q., Zhang X., Wan Q., Wang S., Zhang R., Zhang Z. Transcriptome and microbiome analyses of the mechanisms underlying antibiotic-mediated inhibition of larval development of the saprophagous insect Musca domestica (Diptera: Muscidae). Ecotoxicology and Environmental Safety, 2021, 223: 112602 CrossRef
  7. Lalander C., Senecal J., Calvo M.G., Ahrens L., Josefsson S., Wibergb K., Vinnerås B. Fate of pharmaceuticals and pesticides in fly larvae composting. Science of the Total Environment, 2016, 565: 279-286 CrossRef
  8. Gao Q., Deng W., Gao Z., Li M., Liu W., Wang X., Zhu F. Effect of sulfonamide pollution on the growth of manure management candidate Hermetia illucens. PLoS ONE, 2019, 14(5): e0216086 CrossRef
  9. EFSA Panel on Nutrition, Novel Foods and Food Allergens (NDA), Turck D., Castenmiller J., De Henauw S., Hirsch-Ernst K.I., Kearney J., Maciuk A., Mangelsdorf I., McArdle H.J., Naska A., Pelaez C., Pentieva K., Siani A., Thies F., Tsabouri S., Vinceti M., Cubadda F., Frenzel T., Heinonen M., Marchelli R., Neuhauser-Berthold M., Poulsen M., Prieto Maradona M., Schlatter J.R., van Lovaren H., Ververis E., Knutsen H.K. Safety of dried yellow mealworm (Tenebrio molitor larva) as a novel food pursuant to Regulation (EU) 2015/2283. EFSA Journal, 2021, 19(1): e06343 CrossRef
  10. Khanal P., Pandey D., Næss G., Cabrita A.R.J., Fonseca A.J.M., Maia M.R.G., Timilsina B., Veldkamp T., Sapkota R., Overrein H. Yellow mealworms (Tenebrio molitor) as an alternative animal feed source: a comprehensive characterization of nutritional values and the larval gut microbiome. Journal of Cleaner Production, 2023, 389: 136104 CrossRef
  11. Siow H.S., Sudesh K., Murugan P., Ganesan S. Mealworm (Tenebrio molitor) oil characterization and optimization of the free fatty acid pretreatment via acid-catalyzed esterification. Fuel, 2021, 299: 120905 CrossRef
  12. Nowak V., Persijn D., Rittenschober D., Charrondiere U.R. Review of food composition data for edible insects. Food Chemistry, 2016, 193(15): 39-46 CrossRef
  13. Ramos-Elorduy J., González E.A., Hernández A.R., Pino J.M. Use of Tenebrio molitor (Coleoptera: Tenebrionidae) to recycle organic wastes and as feed for broiler chickens. Journal of Economic Entomology, 2002, 95(1): 214-220 CrossRef
  14. Shaykhiev I.G., Sverguzova S.V., Sapronova Zh.A., Svyatchenko A.V., Ushakova N.A. Vestnik astrakhanskogo gosudarstvennogo tekhnicheskogo universiteta. Seriya: rybnoe khozyaystvo, 2021, 1: 69-81 CrossRef (in Russ.).
  15. Sherman R.A., Wyle F.A., Thrupp L. Effects of seven antibiotics on the growth and development of Phaenicia sericata (Diptera: Calliphoridae) larvae. Journal of Medical Entomology, 1995, 32(5): 646-649 CrossRef
  16. Baguer A.J., Jensen J., Krogh P.H. Effects of the antibiotics oxytetracycline and tylosin on soil fauna. Chemosphere, 2000, 40: 751-757 CrossRef
  17. Aust M.-O., Godlinski F., Travis G.R., Hao X., McAllister T.A., Leinweber P., Thiele-Bruhn S. Distribution of sulfamethazine, chlortetracycline and tylosin in manure and soil of Canadian feedlots after subtherapeutic use in cattle. Environmental Pollution, 2008, 156(3): 1243-1251 CrossRef
  18. Rahmathulla V.K., Nayak P. Effect of antibiotic administration on growth and development of silk gland in mulberry silkworm (Bombyx mori L.). Munis Entomology & Zoology, 2017, 12(1): 41-49.
  19. Ahmad A., Broce A., Zurek L. Evaluation of significance of bacteria in larval development of Cochliomyia macellaria (Diptera: Calliphoridae). Journal of Medical Entomology, 2006, 43: 1129-1133 CrossRef
  20. Preußer D., Bröring U., Fischer T., Juretzek T. Effects of antibiotics ceftriaxone and levofloxacin on the growth of Calliphora vomitoria L. (Diptera: Calliphoridae) and effects on the determination of the post-mortem interval. Journal of Forensic and Legal Medicine, 2021, 81: 102207 CrossRef
  21. Ichikawa T., Kurauchi T. Larval cannibalism and pupal defense against cannibalism in two species of tenebrionid beetles. Zoological Science, 2009, 26(8): 525-529 CrossRef
  22. Jordan H.R., Tomberlin J.K. Microbial influence on reproduction, conversion, and growth of mass produced insects. Current Opinion in Insect Science, 2021, 48: 57-63 CrossRef
  23. Goane L., Salgueiro J., Pereyra P.M., Arce O.E.A., Ruiz M.J., Nussenbaum A.L., Segura D.F., Vera M.T. Antibiotic treatment reduces fecundity and nutrient content in females of Anastrepha fraterculus (Diptera: Tephritidae) in a diet dependent way. Journal of Insect Physiology, 2022, 139: 104396 CrossRef
  24. Ferraz A.C.P., Dallavecchia D.L., Silva D.C., Figueiredo A.L., Proenc B., Silva-Filho R.G., Aguiar V.M. Effects of the antibiotics gentamicin on the postembryonic development of Chrysomya putoria (Diptera: Calliphoridae). Journal of Insect Science, 2014, 14(1): 279 CrossRef
  25. Ben-Yosef M., Aharon Y., Jurkevitch E., Yuval B. Give us the tools and we will do the job: symbiotic bacteria affect olive fly fitness in a diet-dependent fashion. Proceedings of the Royal Society of London. Series B, Biological Sciences, 2010, 277: 1545-1552 CrossRef
  26. Gantner M., Krol K., Piotrowska A., Sionek B., Sadowska A., Kulik K., Wiacek M. Adding mealworm (Tenebrio molitor L.) powder to wheat bread: effects on physicochemical, sensory and microbiological qualities of the end-product. Molecules, 2022, 27: 6155 CrossRef
  27. Kim H.-W., Setyabrata D., Lee Y.J., Jones O.G., Kim Y.H.B. Pre-treated mealworm larvae and silkworm pupae as a novel protein ingredient in emulsion sausages. Innovative Food Science and Emerging Technologies, 2016, 38(A): 116-123 CrossRef
  28. De Marco M., Martinez S., Hernandez F., Madrid J., Gai F., Rotolo L., Belforti M., Bergero D., Katz H., Dabbou S., Kovitvadhi A., Zoccarato I., Gasco L., Schiavone A. Nutritional value of two insect larval meals (Tenebrio molitor and Hermetia illucens) for broiler chickens: apparent nutrient digestibility, apparent ileal amino acid digestibility and apparent metabolisable energy. Animal Feed Science and Technology, 2015, 209: 211-218 CrossRef
  29. Sarica S., Kanoglu B., Yildirim U. Defatted yellow mealworm larvae (Tenebrio molitor l.) meal as possible alternative to fish meal in quail diets. South African Journal of Animal Science, 2020, 50(3): 481-491 CrossRef
  30. Shakeri J., Fos H.A. Proteolytic activity and antibiotic production by Trichoderma harzianum in relation to pathogenicity to insects. Enzyme and Microbial Technology, 2007, 40: 961-968 CrossRef

 

back