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Activity of powdered methylxanthine applied to poultry litter on adults of Alphitobius diaperinus (Panzer, 1797) (Coleoptera: Tenebrionidae)

Abstract

One of the pests that most affect and compromise poultry production worldwide is the insect Alphitobius diaperinus, known as the lesser mealworm. This insect is a vector of diseases that compromise not only chicken production but also human health. This study proposes to examine the efficacy and determine the appropriate rate of methylxanthine (MTX), a natural insecticide extracted from cafeine, for the control of an adult population of lesser mealworms in poultry litter. A total of 2,500 adult mealworms were distributed into five treatments in a completely randomized design using 10 replications with 50 insects per replication. The treatments consisted of a control group and four concentrations of MTX (14, 16, 18, and 20 g/m2) spread in plastic boxes containing reused poultry litter and feed, allocated in a broiler shed, to simulate the farm condition. The experimental period was 18 days, and five readings were performed on days 2, 4, 6, 10, and 18. Methylxanthine affected (P<0.05) the mealworms’ cumulative mortality rate, with the groups of insects housed in boxes treated with 16 g /m2 MTX showing the highest cumulative mortality (86.6%) at the end of the experimental period. In conclusion, MTX has insecticidal action on adults of lesser mealworm and can be used on chicken litter to control the population of this insect in poultry sheds. The MTX concentration of 16 g/m2 showed the greatest effectiveness.

Keywords:
chicken bed; insecticide; lesser mealworm; methylxanthine

Resumo

Uma das pragas que mais afetam e comprometem a produção avícola no mundo é o inseto Alphitobius diaperinus, conhecido como cascudinho. Este inseto é vetor de doenças que comprometem não só a produção de frangos como também a saúde humana. Objetivou-se com esse trabalho avaliar a eficácia e determinar a dose adequada de Metilxantina (MTX), inseticida natural extraído da cafeína, para o controle da população adulta de cascudinhos em cama de frango. Foram utilizados 2.500 cascudinhos adultos distribuídos em delineamento inteiramente casualizado, cinco tratamentos, 10 repetições com 50 insetos por repetição. Os tratamentos consistiram de grupo controle e quatro concentrações 14 g/m2, 16 g/m2, 18 g/m2, 20 g/m2 de MTX espalhadas em recipientes plásticos contendo cama de frango reutilizada e ração, alocados em um galpão de frangos de corte a fm de simular a condição de granja. Período experimental foi de 18 dias e realizadas cinco leituras nos dias dois, quatro, seis, 10 e 18. A MTX afetou (P<0,05) a taxa de mortalidade acumulada de cascudinhos, grupos de insetos alojados em caixas tratadas com 16 g/m2 de MTX apresentaram maior mortalidade acumulada (86,6%) ao final do período experimental. Conclui-se que MTX tem ação inseticida sobre adultos de cascudinho, podendo ser utilizada sobre a cama de frango para o controle da população deste inseto em galpões de criação de frangos, a concentração 16 g/MTX/m2 demonstrou maior efetividade.

Palavras-chave:
Metilxantina; inseticida; cama de frango; cascudinho

Introduction

Alphitobius diaperinus, a beetle commonly known as the lesser mealworm, is one of the most abundant insects in chicken production facilities. The species stands out in the poultry industry for having the status of a pest, as it is a reservoir and vector of pathogens and is difficult to control. The lesser mealworm breeds in litter used on chicken farms and feeds on poultry waste, feed leftovers, broken eggs, dead birds, and other organic materials(11 Volpato A, Galli GM, Campigotto G, Glombowsky P, Santos RCV, Silva AS, Vaucher RA. Avaliação in vitro dos efeitos inseticida e larvicida de oito óleos essenciais sobre o cascudinho aviário (Alphitobius diaperinus). Arch. Vet. Sci. 2018; 23(2):84-90. Available from: http://dx.doi.org/10.5380/avs.v23i2.46127
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). The greatest economic losses in poultry production establishments are due to: i) the preference of birds to consume this insect instead of feed, which reduces their weight gain(44 Santos JC, Alves LFA, Opazo MAU, Mertz NR, Marcomini AM, Oliveira DGP, Bonini AK. Eficiência da aplicação de inseticida químico no solo para o controle de Alphitobius diaperinus Panzer (Coleoptera: Tenebrionidae) em aviário de frango de corte. Arq. Inst. Biol. 2009; 76(3):417-425. Available from: http://dx.doi.org/10.1590/1808-1657v76p4172009
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); ii) damage to the structures of the facilities, as mealworm larvae usually dig tunnels into the walls, insulating materials, and on the foor of the shed in search of places to pupate and escape from the enemies present in the litter(22 Axtell RC, Arends JJ. Ecology and management of arthropod pests of poultry. Annu. Rev. Entomol. 1990; 35(1990):101-126. Available from: https://doi.org/10.1146/annure-v.en.35.010190.000533
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The birds’ health is also compromised because A. diaperinus act as transmission routes for etiological agents of diseases such as: i) Salmonella (1515 McAllister JC, Steelman CD, Skeeles JK. Reservoir competence of the lesser mealworm (Coleoptera: Tenebrionidae) for Salmonella typhimurium (Eubacteriales: Enterobacteriaceae). J. Med. Entomol. 1994; 31(3):369-372. Available from: https://doi.org/10.1093/jmedent/31.3.369
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, 1616 Crippen TL, Zheng L, Sheffield CL, Tomberlin JK, Beier RC, Yu Z. Transient gut retention and persistence of Salmonella through metamorphosis in the lesser mealworm, Alphitobius diaperinus (Coleoptera: Tenebrionidae). J. Appl. Mcrobiol. 2012; 112(5):920-926. Available from: https://dx.doi.org/10.1111/j.1365-2672.2012.05265.x
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, 1717 Roche AJ, Cox NA, Richardson LJ, Buhr RJ, Cason JA, Fairchild BD, Hinkle NC. Transmission of Salmonella to broilers by contaminated larval and adult lesser mealworms, Alphitobius diaperinus (Coleoptera: Tenebrionidae). Poult. Sci. 2009; 88(1):44-48. Available from: https://doi.org/10.3382/ps.2008-00235
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), Campylobacter sp.(1818 Strother KO, Steelman CD, Gbur EE. Reservoir competence of lesser mealworm (Coleoptera: Tenebrionidae) for Campylobacter jejuni (Campylobacterales: Campylobacteraceae). J. Med. Entomol. 2005; 42(1):42-47. Available from: https://doi.org/10.1093/jmedent/42.1.42
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), Escherichia coli(1919 De Las Casas E, Pomeroy BS, Harein PK. Infection and quantitative recovery of Salmonella typhimurium and Escherichia coli from within the lesser mealworm, Alphitobius diaperinus (Panzer). Poult. Sci. 1968; 47(6):1871-1875. Available from: https://doi.org/10.3382/ps.0471871
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,2020 De Las Casas E, Harein PK, Pomeroy BS. Bacteria and fungi within the lesser mealworm collected from poultry brooder houses. Environ. Entomol. 1972; 1(1):27-30. Available from: https://doi.org/10.1093/ee/1.1.27
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,2121 McAllister JC, Steelman CD, Skeeles JK, Newberry LA, Gbur EE. Reservoir competence of the Alphitobius diaperinus (Coleoptera: Tenebrionidae) for Escherichia coli (Eubacteriales: Enterobacteriaceae). J. Med. Entomol. 1996; 33(6):983-987. Available from: https://doi.org/10.1093/jmedent/33.6.983
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); ii) fungi(2020 De Las Casas E, Harein PK, Pomeroy BS. Bacteria and fungi within the lesser mealworm collected from poultry brooder houses. Environ. Entomol. 1972; 1(1):27-30. Available from: https://doi.org/10.1093/ee/1.1.27
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); iii) Marek's disease virus(2222 Eidson CS, Schmittle SC, Goode RB, Lal JB. The role of the darkling beetle (Alphitobius diaperinus) in the transmission of acute leukosis in chickens. Poult. Sci. 1965; 44(5):1366-1367. Available from: https://doi.org/10.3382/ps.0441347
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), Newcastle disease and yaws(2323 De Las Casas E, Harein PK, Deshmukh DR, Pomeroy BS. Relationship between the lesser mealworm, fowl pox and New-castle disease virus in poultry. J. Econ. Entomol. 1976; 69(6):775-779. Available from: https://doi.org/10.1093/jee/69.6.775
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), enteritis(2424 Despins JL, Axtell RC, Rives DV, Guy JS, Ficken MD. Transmission of enteric pathogens of turkeys by darkling beetle larva (Alphitobius diaperinus). J. Appl. Poult. Res. 1994; 3(1):61-65. Available from: https://doi.org/10.1093/japr/3.1.61
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), and Gumboro disease(2525 Watson DW, Guy JS, Stringham SM. Limited transmission of turkey coronavirus in young turkeys by adult Alphitobius diaperinus (Coleoptera: Tenebrionidae). J. Med. Entomol. 2000; 37(3):480-483. Available from: https://doi.org/10.1093/jmedent/37.3.480
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,2626 Mullen G, Durden L. Medical and veterinary entomology. 3 rd ed. San Diego, United States, Academic Press, 2019;794p.); iv) chicken tapeworm(2727 Elowni EE, Elbihari S. Natural and experimental infection on the beetle, Alphitobius diaperinus (Coleoptera: Tenebrionidae) with Choanotaenia infundibulum and other chicken tape-worms. Vet. Sci. Commun. 1979; 3:171-173. Available from: https://doi.org/10.1007/BF02268965
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), and Ascaridia galli(2727 Elowni EE, Elbihari S. Natural and experimental infection on the beetle, Alphitobius diaperinus (Coleoptera: Tenebrionidae) with Choanotaenia infundibulum and other chicken tape-worms. Vet. Sci. Commun. 1979; 3:171-173. Available from: https://doi.org/10.1007/BF02268965
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). The chemical products most widely used are pyrethroids (bifenthrin, deltamethrin, fenitrothion, pirimiphos-methyl), which are highly toxic to birds and whose accumulation in muscle tissue renders the meat of these chickens unsuitable for human consumption(11 Volpato A, Galli GM, Campigotto G, Glombowsky P, Santos RCV, Silva AS, Vaucher RA. Avaliação in vitro dos efeitos inseticida e larvicida de oito óleos essenciais sobre o cascudinho aviário (Alphitobius diaperinus). Arch. Vet. Sci. 2018; 23(2):84-90. Available from: http://dx.doi.org/10.5380/avs.v23i2.46127
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,2828 Galli A, Souza D, Garbellini GS, Coutinho CFB, Mazo LH, Avaca LA, Machado SAS. Utilização de técnicas eletroanalíticas na determinação de pesticidas em alimentos. Quím. Nova. 2006; 29(1):105-112. Available from: https://doi.org/10.1590/S0100-40422006000100020
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). The number of reports of lesser mealworm populations resistant to these compounds is increasing(2929 Tomberlin JK, Richman D, Myers HM. Susceptibility of Alphitobius diaperinus (Coleoptera: Tenebrionidae) from broiler facilities in Texas to four insecticides. J. Econ. Entomol. 2008; 101(2):480-483. Available from: https://doi.org/10.1603/0022-0493(2008)101[480:soadct]2.0.co;2
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, 3030 Chernaki-Lefer AM, Sosagómez DR, Almeida LM, Lopes ION. Susceptibility of Alphitobius diaperinus (Panzer) (Coleoptera, Tenebrionidae) to cypermethrim, dichlorvos and trifumuron in southern Brazil. Rev. Bras. Entomol. 2011; 220(1):125-128. Available from: https://doi.org/10.1590/S0085-56262011000100020
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, 3131 Fogaça I, Ferreira E, Saturnino KC, Santos TR, Cavali J, Porto MO. Álcool para controle de cascudinho em cama de frangos de corte. Arch. Zootec. 2017; 66(256):509-514. Available from: https://doi.org/10.21071/az.v66i256.2766
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), including in Brazil(3232 Chernaki-Lefer AM, Sosa-Gomez DR, Almeida LM. Suscetibilidade de Alphitobius diaperinus (Panzer, 1797) (Coleoptera: Tenebrionidae) a reguladores de crescimento de insetos (RCI). Arq. Inst. Biol. 2006; 73(1):51-55. Available from: https://www.researchgate.net/publication/284549911_Susceptibility_of_Alphitobius_diaperinus_Panzer_1797_Coleoptera_Tenebrionidae_to_insect_growth_regulators_IGR
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,3333 Gazoni FL, Flores F, Bampi RA, Silveira F, Boufeur R, Lovato. Avaliação da resistência do cascudinho (Alphitobius diaperinus) (Panzer) (Coleoptera: Tenebrionidae) a diferentes temperaturas. Arq. Inst. Biol. 2012; 79(1): 69-74. Available from: https://www.scielo.br/j/aib/a/QDGt4PYpcqL76Yt3XtPH5bD/?format=pdf⟨=pt
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).

Chemical control of the lesser mealworm through the application of pyrethroid and organophosphate insecticides is commonly used as a preventive measure(3434 Alves LFA, Uemura-Lima DH, Oliveira DGP, Godinho RPV. Eficiência de um novo inseticida comercial para o controle do cascudinho dos aviários (Alphitobius diaperinus) (Panzer) (Coleoptera: Tenebrionidae). Arq. Inst. Biol. 2010; 77(4):693-700. Available from: https://doi.org/10.1590/1808-1657v77p6932010
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), and this approach during downtime is more efficient for producers in the short term. However, research has already shown that this type of chemical control with the use of pyrethroids in litters during downtime no longer yields effective results due to the return of the presence of this pest during housing(3535 Dias DA, Vargas AB, Almeida FS. Efeitos de dosagem mais concentrada de cipermetrina no controle de cascudinho. Rev. Acad. Ciênc. Agrár. Ambient. 2013; 11(4):437-442. Available from: https://doi.org/10.7213/academico.011.004.AO11
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). In this scenario, the use of natural products is another method that has stood out in the control of several pathogenic microorganisms and pests. These products can be an efficient and viable alternative for the control of the lesser mealworm, since this method does not depend on the absence of birds in the poultry shed. Some essential oils have already been tested and their insecticidal effect proven, e.g. Melaleuca alternifolia oils(11 Volpato A, Galli GM, Campigotto G, Glombowsky P, Santos RCV, Silva AS, Vaucher RA. Avaliação in vitro dos efeitos inseticida e larvicida de oito óleos essenciais sobre o cascudinho aviário (Alphitobius diaperinus). Arch. Vet. Sci. 2018; 23(2):84-90. Available from: http://dx.doi.org/10.5380/avs.v23i2.46127
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,3636 Volpato A, Lorenzetti WR, Zortea T, Giombelli LCDD, Baretta D, Santos RCV, Vaucher RA, Rafin RP, Souza ME, Stefani LM, Boligon AA, Athayde ML, Silva AS. Melaleuca alternifolia essential oil against the lesser mealworm (Alphitobius diaperinus) and its possible effect on the soil fauna. Rev. Bras. Ciênc. Avíc. 2016; 18(1):41-46. Available from: https://doi.org/10.1590/1516-635X1801041-046
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).

Cafeine (1,3,7 trimethylxanthine) is a fatsoluble alkaloid belonging to the class of compounds called methylxanthine(3737 Maria CAB, Moreira RFA. Cafeína: revisão sobre métodos de análise. Quim. Nova. 2007; 30(1):99-105. Available from: http://static.sites.sbq.org.br/quimicanova.sbq.org.br/pdf/Vol30-No19920-RV05372.pdf
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) that acts on the human central nervous system and is also known for its antioxidant properties(3838 Krisko A, Kveder M, Pifat G. Efect of cafeine on oxidation susceptibility of human plasma low density lipoproteins. Clin. Chim. Acta. 2005; 355(1-2):47-53. Available from: https://doi.org/10.1016/j.cccn.2004.12.001
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). Together with theophylline, it is found in wild fruits, seeds, and leaves of numerous plant species including tea, cofee, cocoa, and nuts(3939 Varago FC, Silva LP, Ribeiro JR, Fernandes CA, Carvalho BC, Gioso MM, Moustacas VS. Teoflina como agente capacitante do semen bovino. Arq. Bras. Med. Vet. Zootec. 2017; 69(6): 1670-1614. Available from: https://doi.org/10.1590/1678-4162-9173
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). Studies have shown that cafeine causes toxic effects on Aedes aegypti larvae, interfering with their development and consequently preventing them from reaching the adult stage(4040 Laranja AT, Manzato AJ, Bicudo HEMC. Efects of cafeine and used cofee grounds on biological features of Aedes aegypti (Diptera: Culicidae) and their possible use in alternative control. Genet. Mol. Biol. 2003; 26(4):419-429. Available from: https://doi.org/10.1590/S1415-47572003000400004
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, 4141 Guirado MM, Bicudo HEMMC. Attractiveness of bioinsecticides cafeine and used cofee grounds in the choice of oviposition site by Aedes aegypti (Diptera: Culicidae). Int. J. Mosquito Res. 2016; 47(3):47-51. Available from: https://docs.bvsalud.org/biblioref/ses-sp/2016/ses-38077/ses-38077-7041.pdf
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), which leads to a decrease in oviposition rate(4242 Laranja AT, Manzato AJ, Bicudo HEMC. Cafeine effect on mortality and oviposition in successive generations of Aedes aegypti. Rev. Saúde Pública. 2006; 40(6): 1112-1117. Available from: https://doi.org/10.1590/S0034-89102006000700022
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).

The objective of this study was to examine the efficacy and determine the effective concentration of methylxanthine extracted from cafeine against adults of lesser mealworm (Alphitobius diaperinus) in poultry litter.

Material and methods

The experiment was carried out in the Experimental Poultry House in the Poultry Section of the Animal Science Department of the Veterinary and Animal Science School at the Federal University of Goiás, located in Goiânia - GO, Brazil. A total of 2,500 lesser mealworm (Alphitobius diaperinus) adults captured in several broiler farms in the region of Itaberaí - GO were used in a completely randomized experimental design with five treatments and 10 replications with 50 insects per experimental unit. The treatments consisted of four concentrations of methylxanthine (MTX) (14, 16, 18, and 20 g/m2) spread in plastic boxes (41 × 27 × 12.5 cm) containing a 10-cm-high layer of reused chicken litter with a portion of chicken feed, plus a control group without the use of any product.

After the mealworms and MTX were placed, the boxes were sealed with tulle fabric to prevent the entry and exit of insects. Subsequently, the boxes were transferred to a broiler shed to simulate the farm condition. The experiment lasted 18 days and five readings were performed, on days 2, 4, 6, 10, and 18. At each elapsed period, the seals were removed to count dead and live insects with the aid of surgical tweezers and data were recorded in collection forms. Afterwards, the boxes were sealed again, and this process was repeated until the end of the experimental period. Data were evaluated by analysis of variance (ANOVA) and Tukey's test using the R computer package and adopting α=0.05.

Results

The methylxanthine (MTX) concentration affected (P<0.05) the cumulative mortality rate of lesser mealworm. The groups of insects housed in boxes treated with 16 g MTX/m2 showed the highest cumulative mortality (86.6%) at the end of the experimental period (Table 1).

Table 1
Cumulative mortality rate of lesser mealworm (Alphitobius diaperinus) in chicken litter treated with methylxanthine (MTX)

Discussion

The primary effect of methylxanthine (MTX) in the mealworm was found to be due to the inhibition of phosphodiesterase activity and intracellular increase of cyclic adenosine monophosphate (cyclic AMP). At low concentrations, they are potent synergists of other insecticides known to activate adenylate cyclase in insects. These data suggest the use of MTX in the control of arthropods as a natural insecticide, by inhibiting phosphodiesterase alone with the involvement of AMP cyclase; or in combination with other compounds(4343 Nathanson JA. Cafeine and related methylxanthines: possible naturally occurring pesticides. Science. 1984; 226(4671): 184-187. Available from: https://doi.org/10.1126/science.6207592
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). Nathanson(4343 Nathanson JA. Cafeine and related methylxanthines: possible naturally occurring pesticides. Science. 1984; 226(4671): 184-187. Available from: https://doi.org/10.1126/science.6207592
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) demonstrated the pesticidal and pestistatic activity of MTX in goliath worm (Manduca sexta) larvae and observed lethality within 24 h. Polo(4444 Pólo AM. Efeito da cafeína no desenvolvimento de Aedes aegypti (Diptera: Culicidae): o significado biológico das alterações do padrão de síntese de esterases. Dissertação Mestrado. UNESP, 2014. Available from: http://www.sbicafe.ufv.br/hand-le/123456789/8993
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) showed that MTX alters the synthesis pattern of esterases, which are important in several physiological processes and are even involved in blocking insect metamorphosis. Esterases are also involved in several physiological processes, including neuronal activity(4545 Harel M, Kryger G, Rosenberry TL, Mallender WD, Lewis T, Fletcher RJ, Guss JM, Silman I, Sussman JL. Three-dimensional structures of Drosophila melanogaster acetylcholinesterase and of its complexes. Protein Sci. 2000; 9(6):1063-1072. Available from: https://dx.doi.org/10.1110%2Fps.9.6.1063
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), insect juvenile hormone metabolism(4646 Davey K. The interaction of feeding and mating in the hormonal control of egg production in Rhodnius prolixus. J. Insect Physiol. 2007; 53(3): 208-215. Available from: https://doi.org/10.1016/j.jinsphys.2006.10.002
https://doi.org/10.1016/j.jinsphys.2006....
), and insecticide resistance(4747 Lucena ALM, Gigliolli AAS, Lapenta AS. Análise das esterases durante as fases do desenvolvimento em Sitophilus oryzae (Coleoptera: Curculionidae) e sua relação com a resistência ao inseticida malathion. SaBios: Rev. Saúde Biol. 2012; 7(3):36-44. Available from: https://revista2.grupointegrado.br/revista/index.php/sabios/article/view/771
https://revista2.grupointegrado.br/revis...
).

In neuronal activity, acetylcholine is released into the synaptic cleft, binds to transmembrane receptors, and generates signal transmission. Later, acetylcholinesterase hydrolyzes acetylcholine, triggering the stimulus(4848 Pohanka M. Alpha-7-nicotinic acetylcholine receptor is a target in pharmacology and toxicology. Int. J. Mol. Sci. 2012; 13(2):2219-2238. Available from: https://dx.doi.org/10.3390%2Fijms13022219
https://dx.doi.org/10.3390%2Fijms13022219...
). Nishi et al.(4949 Nishi Y, Sasaki K, Miyatake T. Biogenic amines, cafeine and tonic immobility in Tribolium castaneum. J. Insect Physiol. 2010; 56(6):622-628. Available from: https://doi.org/10.1016/j.jinsphys.2010.01.002
https://doi.org/10.1016/j.jinsphys.2010....
) confirmed that cafeine inhibits the pattern of esterase gene expression. Juvenile hormone esterase controls the concentration of juvenile hormone and, therefore, cafeine alters the gene expression pattern of esterases. Juvenile hormone is a class of sesquiterpenoids produced in the insect Corpora Allata and distributed throughout the hemolymph, being directly involved in several metabolic activities of insects such as metamorphosis and oogenesis. During metamorphosis, it modulates ecdysteroid activity (20E), preventing molt from occurring during the larval stage(5050 Mansur JF, Figueira-Mansur J, Santos AS, Santos-Junior H, Ramos IB, Medeiros MN, Machado EA, Kaiser CR, Muthukrishnan S, Masuda H, Melo ACA, Moreira MF. The effect of lufenuron, a chitin synthesis inhibitor, on oogenesis of Rhodnius prolixus. Pestic. Biochem. Physiol. 2010; 98(1):59-67. Available from: http://dx.doi.org/10.1016/j.pestbp.2010.04.013
http://dx.doi.org/10.1016/j.pestbp.2010....
).

Among the different plant extracts with insecticidal effect demonstrated in laboratory studies, cafeine has been the one that acts in the intoxication of larvae, interrupting their development and leading them to death(4040 Laranja AT, Manzato AJ, Bicudo HEMC. Efects of cafeine and used cofee grounds on biological features of Aedes aegypti (Diptera: Culicidae) and their possible use in alternative control. Genet. Mol. Biol. 2003; 26(4):419-429. Available from: https://doi.org/10.1590/S1415-47572003000400004
https://doi.org/10.1590/S1415-4757200300...
,4242 Laranja AT, Manzato AJ, Bicudo HEMC. Cafeine effect on mortality and oviposition in successive generations of Aedes aegypti. Rev. Saúde Pública. 2006; 40(6): 1112-1117. Available from: https://doi.org/10.1590/S0034-89102006000700022
https://doi.org/10.1590/S0034-8910200600...
,5151 Guirado MM, Bicudo HEMC. Efect of used cofee grounds on larval mortality of Aedes aegypti L. (Díptera: culicidae): Suspension concentration and age versus efficacy. BioAssay. 2007; 2(5):1-7. Available from: http://www.seb.org.br/biosay/arquivos/journals/1/articles/52/public/52-254-1-PB.pdf
http://www.seb.org.br/biosay/arquivos/jo...
). Cafeine proved to be potentially effective in controlling adult red four beetles through repellent, fumigant, and contact effects, and its action is believed to be linked to the inhibition of certain enzymes such as carboxylesterase(5252 Phankaen Y, Manaprasertsak A, Pluempanupat W, Koul O, Kainoh Y, Bullangpoti V. Toxicity and repellent action of Coffea arabica against Tribolium castaneum (Herbst) adults under laboratory conditions. J. Stored Prod. Res. 2017; 71(2017):112-118. Available from: https://doi.org/10.1016/j.jspr.2017.01.006
https://doi.org/10.1016/j.jspr.2017.01.0...
). In adult insects, cafeine causes motor immobility by increasing the activity of the dopamine receptor, an antagonist of adenosine receptors, inhibiting their action(4949 Nishi Y, Sasaki K, Miyatake T. Biogenic amines, cafeine and tonic immobility in Tribolium castaneum. J. Insect Physiol. 2010; 56(6):622-628. Available from: https://doi.org/10.1016/j.jinsphys.2010.01.002
https://doi.org/10.1016/j.jinsphys.2010....
,5353 Fredholm BB, Bättig K, Holmén J, Nehlig A, Zvartau EZ. Actions of cafeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol. Rev. 1999; 51(1):83-133. Available from: https://pharmrev.aspetjournals.org/content/51/1/83
https://pharmrev.aspetjournals.org/conte...
,5454 Zahniser N, Simosky JK, Mayfield RD, Negri CA, Hanania T, Larson GA, Kelly MA, Grandy DK, Rubinstein M, Low MJ, Fredholm BB. Functional uncoupling of adenosine A(2A) receptors and reduced response to cafeine in mice lacking dopamine D2 receptors. J. Neurosci. 2000; 20(16):5949-5957. Available from: https://doi.org/10.1523/jneurosci.20-16-05949.2000
https://doi.org/10.1523/jneurosci.20-16-...
). Cafeine acts in a dose-dependent manner, with the concentration of 1 mg/mL of water being lethal to larvae(4040 Laranja AT, Manzato AJ, Bicudo HEMC. Efects of cafeine and used cofee grounds on biological features of Aedes aegypti (Diptera: Culicidae) and their possible use in alternative control. Genet. Mol. Biol. 2003; 26(4):419-429. Available from: https://doi.org/10.1590/S1415-47572003000400004
https://doi.org/10.1590/S1415-4757200300...
).

Herbal products are recognized as natural insecticides, as is the case of tea extract-based emulsion, which can be used as an insecticide to control the green peach aphid(5858 Khoshraftar Z, Shamel A, Safekordi AA, Zaefzadeh M. Chemical composition of an insecticidal hydroalcoholic extract from tea leaves against green peach aphid. Int. J. Environ. Sci. Technol. 2019; 16(11):7583-7590. Available from: http://dx.doi.org/10.1007/s13762-018-2177-x
http://dx.doi.org/10.1007/s13762-018-217...
). Some formulations of insecticides based on medicinal herbs were effective in combating several pests, e.g. rosemary-pepper(5959 Gomes GA, Monteiro CMO, Julião LS, Maturano R, Senra TOS, Zeringóta V, Calmon F, Matos RS, Daemon E, Carvalho MG. Acaricidal activity of essential oil from Lippia sidoides on unengorged larvae and nymphs of Rhipicephalus sanguineus (Acari: Ixodidae) and Amblyomma cajennense (Acari: Ixodidae). Exp. Parasitol. 2014; 137(0):41-45. Available from: https://doi.org/10.1016/j.exppara.2013.12.003
https://doi.org/10.1016/j.exppara.2013.1...
), neem (Azadirachta indica)(6060 Boursier CM, Bosco D, Coulibaly A, Negre M. Are traditional neem extract preparations as efficient as a commercial formulation of azadirachtin A?. Crop Prot. 2011; 30(3):318-322. Available from: https://doi.org/10.1016/j.cropro.2010.11.022
https://doi.org/10.1016/j.cropro.2010.11...
, 6161 Anjali CH, Sharma Y, Mukherjee A, Chandrasekaran N. Neem oil (Azadirachta indica) nanoemulsion--a potent larvicidal agent against Culex quinquefasciatus. Pest Manag. Sci. 2012; 68(2):158-163. Available from: https://doi.org/10.1002/ps.2233
https://doi.org/10.1002/ps.2233...
), garlic(6262 Yang Z, Baldermann S, Watanabe N. Recent studies of the volatile compounds in tea. Food Res. Int. 2013; 53(2):585-599. Available from: https://doi.org/10.1016/j.foodres.2013.02.011
https://doi.org/10.1016/j.foodres.2013.0...
), and several species of eucalyptus(6363 Filomeno CA, Barbosa LCA, Teixeira RR, Pinheiro AL, Farias ES, Silva EMP, Picanço MC. Corymbia spp. and Eucalyptus spp. essential oils have insecticidal activity against Plutella xylostella. Ind. Crops Prod. 2017; 109(0):374-383. Available from: http://dx.doi.org/10.1016/j.indcrop.2017.08.033
http://dx.doi.org/10.1016/j.indcrop.2017...
), whose main deleterious effects in the fght against insects are related to methylxanthine.

In a similar study, Ananenka(6464 Ananenka A. Insecticides and invertebrate neurophysiology: testing the efficacy of cafeine as an insecticide. 2018. Thesis (PhD in Biology). Montreal: Concordia University, 2018. Available from: https://digitalcommons.csp.edu/cup_commons_undergrad/1240
https://digitalcommons.csp.edu/cup_commo...
) tested the efficacy of a natural insecticide composed of cafeine on the house cricket (Acheta domesticus) and concluded that cafeine results in increased neuronal activity and consequently the death of the insect due to depolarization of neurons in the brain membrane, constituting an option to control this species. In the present study, the MTX concentration of 16 g/m2 had positive results for cumulative mortality rate in the total observation period, which was 80% higher than in the control treatment, and ensured a consecutive increase in mortality from the 2nd to the 18th day of observation.

The control of Alphitobius diaperinus is essential due to its many detrimental effects on the productivity of these animals, as this species can cause superficial wounds and negatively affect the birds’ growth. In addition, the ingestion of large amounts of A. diaperinus compromises the nutritional quality of diets, since adults and larvae can cause intestinal obstruction in broilers due to the lack of chitinase for the digestion of chitin, which is widely found in the exoskeleton of the mealworm. This results in necrotic enteritis, reduced nutrient absorption, and, ultimately, considerable economic losses for the poultry industry(6565 Tamburro M, Sammarco ML, Trematerra P, Colacci M, Ripabelli G. Potential role of Alphitobius diaperinus Panzer (Insecta, Coleoptera) in poultry farm as transmission vector of bacterial pathogens in broilers and humans. J. Appl. Microb. 2022; 74(6):883-892. Available from: https://doi.org/10.1111/lam.13679
https://doi.org/10.1111/lam.13679...
, 6666 Rumbos C, Pantazis I, Athanassiou C. Population growth of the lesser mealworm, Alphitobius diaperinus (Panzer) (Coleoptera: Tenebrionidae), on various commodities. J. Econ. Entomol. 2020; 113:1001-1007. Available from: https://doi.org/10.1093/jee/toz313
https://doi.org/10.1093/jee/toz313...
).

Several studies have demonstrated that cypermethrin, dichlorvos, and trifumuron are efficient in controlling ectoparasites in poultry production in Brazil(6767 Oliveira DGP, Cardoso RR, Mamprim AP, Angeli LF. Laboratory and field evaluation of a cypermethrin-based insecticide for the control of Alphitobius diaperinus Panzer (Coleoptera: Tenebrionidae) and its in-vitro effects on Baeauveria bassiana bals. vuill. (Hypocreales: Cordycipitaceae). Braz. J. Poult. Sci. 2016; 18(3):371-380. Available from: https://dx.doi.org/10.1590/1806-9061-2015-0115.
https://dx.doi.org/10.1590/1806-9061-201...
,6868 Souza CJ, Barbosa FM, Marujo MM, Santos ET, Domingues CH, Oliveira D, Sgavioli S. Efect of cypermethrin on the control of lesser mealworm (Alphitobius diaperinus) and broiler performance. Pesq. Vet. Bras. 2021; 41:e06859. Available from: https://doi.org/10.1590/1678-5150-PVB-6859
https://doi.org/10.1590/1678-5150-PVB-68...
). However, resistance of pest populations to these compounds has already been reported in various countries(6969 Tomberlin JK, RichmanD, Myers H. Susceptibility of Alphitobius diaperinus (Coleoptera: Tenebrionidae) from broiler facilities in Texas to four insecticides. J. Econ. Entomol. 2008; 101(2):480-483. Available from: https://dx.doi.org/10.1603/0022-0493
https://dx.doi.org/10.1603/0022-0493...
,7070 Hickmann F, Morais AF, Bronzatto ES, Giacomelli T, Guedes JVC, Bernardi O. Susceptibility of the lesser mealworm, Alphitobius diaperinus (Coleoptera: Tenebrionidae), from broiler farms of southern Brazil to insecticides. J. Econ. Entomol. 2018; 111(2):980-985. Available from: https://dx.doi.org/10.1093/jee/toy059
https://dx.doi.org/10.1093/jee/toy059...
). Therefore, the use of plant extracts such as citronella, cafeine, among others that have an insecticidal action on the central nervous system of insects, is encouraged. These compounds have been proven to harm the development of insects and have repellent and larvicidal activity(7171 Gurib-Fakim A. Medicinal plants: traditions on yesterday and drugs of tomorrow. Mol. Aspects Med. 2006; 27(1):1-93. Available from: https://dx.doi.org/10.1016/j.mam.2005.07.008
https://dx.doi.org/10.1016/j.mam.2005.07...
,7272 López MD, Pascual-Villalobos MJ. Mode of inhibition of acetylcholinesterase by monoterpenoids and implications for pest control. Indust. Crops. Products. 2010; 31(2):284-288. Available from: https://dx.doi.org/10.1016/j.ind-crop.2009.11.005
https://dx.doi.org/10.1016/j.ind-crop.20...
), thereby constituting efficient ways to control the damage caused by Alphitobius diaperinus in poultry production.

Conclusion

Methylxanthine, extracted from cafeine, has an insecticidal action on lesser mealworm (Alphitobius diaperinus) adults and can be used on chicken litter to control the population of this insect in poultry sheds. For this purpose, the methylxanthine concentration of 16 g/m2 is the most effective.

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Publication Dates

  • Publication in this collection
    07 Nov 2022
  • Date of issue
    2022

History

  • Received
    28 Apr 2022
  • Accepted
    02 Sept 2022
  • Published
    30 Sept 2022
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