Effects of biphenyl on Blaberus craniifer (Blattodea, Blaberidae) cockroaches and their parasites – gregarines and nematodes
Keywords:
Blattodea; Thelastomatidae; Eugregarinorida; food supplements; gregarines; xenobiotics; biphenyl; parasitic system; insect parasites.
Abstract
In natural ecosystems, parasites and their hosts are subject to xenobiotics, which overall weaken either a host or its parasites. There has been no laboratory study of this process on the example of cockroaches and their parasites. In accurately controlled conditions, we examined the influence of a food supplement – biphenyl – on cockroaches and their three parasites. In the conditions of our experiment, Blaberus cranifer (Blattodea, Blaberidae) cockroaches significantly reduced the rates of anabolism even while consuming the lowest biphenyl concentration in their diet. While the control group was observed to have a 59.4 mg/day increase in body mass, the mass of the cockroaches given biphenyl in the dose of 0.5% of diet mass decreased by 3.4 mg/day on average. Subject to high dosages of biphenyl (0.5–16.0% of fodder mass), body mass of the cockroaches decreased on average by 1.1–9.4 mg/day. The insects consumed their diet at the same rate, no matter the biphenyl concentration given. The number of gregarines Blabericola cubensis (Eugregarinorida, Blabericolidae) and Protomagalhaensia granulosae did not change even at the highest concentration (16.0% of fodder mass) added to the B. craniifer cockroaches’ diet. We observed no significant changes in the amount of larvae of the Cranifera cranifera (Oxyurida, Thelastomatidae) nematodes, while the adult nematodes tended to decline in number when subject to increased concentration of the food supplement in the cockroaches’ food. The number of P. granulosae gregarines did not significantly increase with body-mass gains of their hosts – cockroaches, that is despite increase in volume of their living environment (the midgut of cockroaches) and extension of the period during which the cockroaches consumed gregarine oocysts from the environment with food. Similarly, the number of B. cubensis gregarines also did not significantly change with increased food consumption by the cockroaches. However, we observed a tendency towards greater numbers of this gregarine in the cockroach larvae that were losing mass during the experiment. The greatest mass loss during the experiment was observed in the cockroaches that consumed biphenyl in the diet and had the largest number of C. cranifera nematodes in the hindgut. We observed no significant negative correlation between the numbers of B. cubensis and P. granulosae gregarines. A cockroach that was found to have 70 specimens of B. cubensis in the midgut, had no P. granulosae gregarines. In contrast, when the intestines of a cockroach contained over 10–15 specimens of P. granulosae, some B. cubensis were always present. The number of C. cranifera nematodes in the cockroaches’ hindgut did not depend on the number of B. cubensis or P. granulosae gregarines in their hosts’ midgut. Perhaps, this was related to absence of competition for the intestinal section among them. The regularities we found are different from what we expected to see in the parasitic system prior to the experiment. Gregarines did not compete with nematodes. Neither of them died from biphenyl, though the cockroaches ceased to normally gain weigh when eating biphenyl. That is, the host suffered from biphenyl more than the parasites, even when consuming the lowest concentration of the xenobiotic we tested.References
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Aron-Wisnewsky, J., Doré, J., & Clement, K. (2012). The importance of the gut microbiota after bariatric surgery. Nature Reviews Gastroenterology and Hepatology, 9(10), 590–598.
Bilan, M. V., Lieshchova, M. A., Tishkina, N. M., & Brygadyrenko, V. V. (2019). Combined effect of glyphosate, saccharin and sodium benzoate on the gut microbiota of rats. Regulatory Mechanisms in Biosystems, 10(2), 228–232.
Boyko, A. A., & Brygadyrenko, V. V. (2017). Changes in the viability of the eggs of Ascaris suum under the influence of flavourings and source materials approved for use in and on foods. Biosystems Diversity, 25(2), 162–166.
Boyko, O. O., & Brygadyrenko, V. V. (2019a). The impact of acids approved for use in foods on the vitality of Haemonchus contortus and Strongyloides papillosus (Nematoda) larvae. Helminthologia, 56(3), 202–210.
Boyko, O. O., & Brygadyrenko, V. V. (2019b). The viability of Haemonchus contortus (Nematoda, Strongylida) and Strongyloides papillosus (Nematoda, Rhabditida) larvae exposed to various flavourings and source materials used in food production. Vestnik Zoologii, 53(6), 433–442.
Boyko, O., & Brygadyrenko, V. (2022). Nematicidal activity of organic food additives. Diversity, 14, 615.
Brygadyrenko, V. V., & Reshetniak, D. Y. (2016). Morphometric variability of Clitellocephalus ophoni (Eugregarinida, Gregarinidae) in the intestines of Harpalus rufipes (Coleoptera, Carabidae). Archives of Biological Sciences, 68(3), 587–601.
Brygadyrenko, V. V., & Svyrydchenko, A. O. (2015). Influence of the gregarine Stenophora julipusilli (Eugregarinorida, Stenophoridae) on the trophic activity of Rossiulus kessleri (Diplopoda, Julidae). Folia Oecologica, 42(1), 10–20.
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Clopton, R. E. (2010). Protomagalhaensia cerastes n. sp. (Apicomplexa: Eugregarinida: Blabericolidae) parasitizing the pallid cockroach, Phoetalia pallida (Dictyoptera: Blaberidae). Comparative Parasitology, 77, 117–124.
Clopton, R. E. (2011). Redescription of Protomagalhaensia granulosae Peregrine, 1970 (Apicomplexa: Eugregarinida: Blabericolidae) parasitizing the discoid cockroach, Blaberus discoidalis (Dictyoptera: Blaberidae). Comparative Parasitology, 78(1), 63–72.
Clopton, R. E. (2012a). Redescription of Protomagalhaensia blaberae Peregrine, 1970 (Apicomplexa: Eugregarinida: Blabericolidae) parasitizing the Bolivian cockroach, Blaberus boliviensis (Dictyoptera: Blaberidae). Comparative Parasitology, 79(2), 182–191.
Clopton, R. E. (2012b). Synoptic revision of Blabericola (Apicomplexa: Eugregarinida: Blabericolidae) parasitizing blaberid cockroaches (Dictyoptera: Blaberidae), with comments on delineating gregarine species boundaries. Jour-nal of Parasitology, 98(3), 572–583.
Clopton, R. E., & Hays, J. J. (2006). Revision of the genus Protomagalhaensia and description of Protomagalhaensia wolfi n. comb. (Apicomplexa: Eugregarinida: Hirmocystidae) and Leidyana haasi n. comb. (Apicomplexa: Eugregarinida: Leidyanidae) parasitizing the lobster cockroach, Nauphoeta cinerea (Dictyoptera: Blaberidae). Comparative Parasitology, 73, 137–156.
Desportes, I., & Schrével, J. (2013). Treatise on zoology – anatomy, taxonomy, biology. The gregarines. In 2 vols. The early branching Apicomplexa. Brill.
Feinberg, M., Soler, L., Contenot, S., & Verger, P. (2011). Assessment of seasonality in exposure to dioxins, furans and dioxin-like PCBs by using long-term food-consumption data. Food Additives and Contaminants: Part A, 28(4), 502–512.
Goudey-Perrière, F., Lemonnier, F., Bergougnoux, V., & Perrière, C. (2007). Low doses of the pesticide lindane induce protein release by the fat body of female cockroach Blaberus craniifer (Dictyoptera). Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 146(4), 492–501.
Goudey-Perrière, F., Lemonnier, F., Perrière, C., Dahmani, F.-Z., & Wimmer, Z. (2003). Is the carbamate juvenoid W-328 an insect growth regulator for the cockroach Blaberus craniifer Br. (Insecta, Dictyoptera)? Pesticide Biochemistry and Physiology, 75, 47–59.
Griesbaum, K., Behr, A., Biedenkapp, D., Voges, H., Garbe, D., Paetz, C., Collin, G., Mayer, D., & Höke, H. (2012). Hydrocarbons. In: Ullmann’s encyclopedia of industrial chemistry. Wiley-VCH, Weinheim. Pp. 168–171.
Grimm, F. A., Hu, D., Kania-Korwel, I., Lehmler, H. J., Ludewig, G., Hornbuckle, K. C., Duffel, M. W., Bergman, Å., & Robertson, L. W. (2015). Metabolism and metabolites of polychlorinated biphenyls. Critical Reviews in Toxicology, 45(3), 245–272.
Halkin, B. M., & Filipova, T. O. (2020). Biotransformacija ksenobiotikov mikrobiotoj zheludochno-kishechnogo trakta i ejo posledstvija dlia cheloveka [Biotransformation of the xenobiotics by microbiota of the gastrointestinal tract and its consequences for humans]. Microbiology and Biotechnology, 49, 6–23 (in Russian).
Koppel, N., Maini Rekdal, V., & Balskus, E. P. (2017). Chemical transformation of xenobiotics by the human gut microbiota. Science, 356(6344), eaag2770.
Kozak, V. M., Romanenko, E. R., & Brygadyrenko, V. V. (2020). Influence of herbicides, insecticides and fungicides on food consumption and body weight of Rossiulus kessleri (Diplopoda, Julidae). Biosystems Diversity, 28(3), 272–280.
Kulma, M., Kouřimská, L., Homolková, D., Božik, M., Plachý, V., & Vrabec, V. (2020). Effect of developmental stage on the nutritional value of edible insects. A case study with Blaberus craniifer and Zophobas morio. Journal of Food Composition and Analysis, 92, 103570.
Lambiase, S., Rasola, M., & Grigolo, A. (2004). Daily rhythm, ATP concentration and oxidative activity in an aposymbiotic strain of Blaberus craniifer Burmeister (Blattaria, Blaberidae). Italian Journal of Zoology, 71(4), 305–308.
Lange, C. E., & Lord, J. C. (2012). Chapter. 10. Protistan entomopathogens. In: Vega, F. E., & Kaya, H. K. (Eds.). Insect pathology. Second edition. Academic Press, Amsterdam. Pp. 367–394.
Lieshchova, M. A., Bilan, M. V., Bohomaz, A. A., Tishkina, N. M., & Brygadyrenko, V. V. (2020). Effect of succinic acid on the organism of mice and their intestinal microbiota against the background of excessive fat consumption. Regulatory Mechanisms in Biosystems, 11(2), 153–161.
Lieshchova, M. A., Tishkina, N. M., Bohomaz, A. A., Gavrilin, P. M., & Brygadyrenko, V. V. (2018). Combined effect of glyphosphate, saccharin and sodium benzoate on rats. Regulatory Mechanisms in Biosystems, 9(4), 591–597.
Lieshchova, M., Logvinova, V., Bilan, M., Bohomaz, A., & Brygadyrenko, V. (2023). Effect of azodicarbonamide on rats with a high-fat hypercaloric diet. Acta Fytotechnica et Zootechnica, 26(1), 15–27.
Martynov, V. O., & Brygadyrenko, V. V. (2017). The influence of synthetic food additives and surfactants on the body weight of larvae of Tenebrio molitor (Coleoptera, Tenebrionidae). Biosystems Diversity, 25(3), 236–242.
Martynov, V. O., & Brygadyrenko, V. V. (2018). The influence of the synthetic food colourings tartrazine, allura red and indigo carmine on the body weight of Tenebrio molitor (Coleoptera, Tenebrionidae) larvae. Regulatory Mechanisms in Biosystems, 9(4), 479–484.
Morffe, J., García, N., Véliz, L., Hasegawa, K., & Carreno, R. A. (2022). Morphological and molecular characterization of two species of nematodes (Oxyuridomorpha: Thelastomatoidea: Protrelloididae, Thelastomatidae) parasitic in the cockroach Blaberus discoidalis Serville (Blattaria: Blaberidae) from Cuba. Zootaxa, 5194(1), 92–108.
Parhomenko, O. V., Kolomiichuk, S. V., Omelianov, D. D., & Brygadyrenko, V. V. (2022). Potential use of synthetic and natural aromatic mixtures in prevention from Shelfordella lateralis сockroaches. Regulatory Mechanisms in Biosystems, 13(2), 174–179.
Parhomenko, O. V., Lagutenko, O. T., Lebedynets, N. V., & Brygadyrenko, V. V. (2023). Body-weight gains in Blaberus craniifer cockroaches and the intensity of their infection with gregarines and nematodes. Biosystems Diversity, 31(3), 368–375.
Schecter, A., Colacino, J., Haffner, D., Patel, K., Opel, M., Päpke, O., & Birnbaum, L. (2010). Perfluorinated compounds, polychlorinated biphenyls, and organochlorine pesticide contamination in composite food samples from Dallas, Texas, USA. Environmental Health Perspectives, 118(6), 796–802.
Sender, R., Fuchs, S., & Milo, R. (2016). Revised estimates for the number of human and bacteria cells in the body. PLoS Biology, 14(8), e1002533.
Smith, A. J., & Cook, T. J. (2008). Host specificity of five species of Eugregarinida among six species of cockroaches (Insecta: Blattodea). Comparative Parasitology, 75(2), 288–291.
Tanada, Y., & Kaya, H. K. (1993). Insect pathology. Academic Press, San Diego.
Yanovych, D. O., & Yanovych, N. E. (2011). Biotransformatsija ksenobiotykiv i mekhanizmy yiyi rehulyatsiyi [Biotransformation of xenobiotics and mechanisms of its regulation]. Scientific Bulletin of the LNUVMBT named after S. Z. Gzhitskyi, 48(2), 305–311 (in Ukrainian).
Aron-Wisnewsky, J., Doré, J., & Clement, K. (2012). The importance of the gut microbiota after bariatric surgery. Nature Reviews Gastroenterology and Hepatology, 9(10), 590–598.
Bilan, M. V., Lieshchova, M. A., Tishkina, N. M., & Brygadyrenko, V. V. (2019). Combined effect of glyphosate, saccharin and sodium benzoate on the gut microbiota of rats. Regulatory Mechanisms in Biosystems, 10(2), 228–232.
Boyko, A. A., & Brygadyrenko, V. V. (2017). Changes in the viability of the eggs of Ascaris suum under the influence of flavourings and source materials approved for use in and on foods. Biosystems Diversity, 25(2), 162–166.
Boyko, O. O., & Brygadyrenko, V. V. (2019a). The impact of acids approved for use in foods on the vitality of Haemonchus contortus and Strongyloides papillosus (Nematoda) larvae. Helminthologia, 56(3), 202–210.
Boyko, O. O., & Brygadyrenko, V. V. (2019b). The viability of Haemonchus contortus (Nematoda, Strongylida) and Strongyloides papillosus (Nematoda, Rhabditida) larvae exposed to various flavourings and source materials used in food production. Vestnik Zoologii, 53(6), 433–442.
Boyko, O., & Brygadyrenko, V. (2022). Nematicidal activity of organic food additives. Diversity, 14, 615.
Brygadyrenko, V. V., & Reshetniak, D. Y. (2016). Morphometric variability of Clitellocephalus ophoni (Eugregarinida, Gregarinidae) in the intestines of Harpalus rufipes (Coleoptera, Carabidae). Archives of Biological Sciences, 68(3), 587–601.
Brygadyrenko, V. V., & Svyrydchenko, A. O. (2015). Influence of the gregarine Stenophora julipusilli (Eugregarinorida, Stenophoridae) on the trophic activity of Rossiulus kessleri (Diplopoda, Julidae). Folia Oecologica, 42(1), 10–20.
Clopton, R. E. (2002). Phylum Apicomplexa Levine, 1970: Order Eugregarinorida Leger, 1900. In: Lee, J. J., Leedale, G., Patterson, D., & Bradbury, P. C. (eds.). Illustrated guide to the Protozoa. 2nd ed. Society of Protozoologists, Lawrence, Kansas. Pages 205–288.
Clopton, R. E. (2010). Protomagalhaensia cerastes n. sp. (Apicomplexa: Eugregarinida: Blabericolidae) parasitizing the pallid cockroach, Phoetalia pallida (Dictyoptera: Blaberidae). Comparative Parasitology, 77, 117–124.
Clopton, R. E. (2011). Redescription of Protomagalhaensia granulosae Peregrine, 1970 (Apicomplexa: Eugregarinida: Blabericolidae) parasitizing the discoid cockroach, Blaberus discoidalis (Dictyoptera: Blaberidae). Comparative Parasitology, 78(1), 63–72.
Clopton, R. E. (2012a). Redescription of Protomagalhaensia blaberae Peregrine, 1970 (Apicomplexa: Eugregarinida: Blabericolidae) parasitizing the Bolivian cockroach, Blaberus boliviensis (Dictyoptera: Blaberidae). Comparative Parasitology, 79(2), 182–191.
Clopton, R. E. (2012b). Synoptic revision of Blabericola (Apicomplexa: Eugregarinida: Blabericolidae) parasitizing blaberid cockroaches (Dictyoptera: Blaberidae), with comments on delineating gregarine species boundaries. Jour-nal of Parasitology, 98(3), 572–583.
Clopton, R. E., & Hays, J. J. (2006). Revision of the genus Protomagalhaensia and description of Protomagalhaensia wolfi n. comb. (Apicomplexa: Eugregarinida: Hirmocystidae) and Leidyana haasi n. comb. (Apicomplexa: Eugregarinida: Leidyanidae) parasitizing the lobster cockroach, Nauphoeta cinerea (Dictyoptera: Blaberidae). Comparative Parasitology, 73, 137–156.
Desportes, I., & Schrével, J. (2013). Treatise on zoology – anatomy, taxonomy, biology. The gregarines. In 2 vols. The early branching Apicomplexa. Brill.
Feinberg, M., Soler, L., Contenot, S., & Verger, P. (2011). Assessment of seasonality in exposure to dioxins, furans and dioxin-like PCBs by using long-term food-consumption data. Food Additives and Contaminants: Part A, 28(4), 502–512.
Goudey-Perrière, F., Lemonnier, F., Bergougnoux, V., & Perrière, C. (2007). Low doses of the pesticide lindane induce protein release by the fat body of female cockroach Blaberus craniifer (Dictyoptera). Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 146(4), 492–501.
Goudey-Perrière, F., Lemonnier, F., Perrière, C., Dahmani, F.-Z., & Wimmer, Z. (2003). Is the carbamate juvenoid W-328 an insect growth regulator for the cockroach Blaberus craniifer Br. (Insecta, Dictyoptera)? Pesticide Biochemistry and Physiology, 75, 47–59.
Griesbaum, K., Behr, A., Biedenkapp, D., Voges, H., Garbe, D., Paetz, C., Collin, G., Mayer, D., & Höke, H. (2012). Hydrocarbons. In: Ullmann’s encyclopedia of industrial chemistry. Wiley-VCH, Weinheim. Pp. 168–171.
Grimm, F. A., Hu, D., Kania-Korwel, I., Lehmler, H. J., Ludewig, G., Hornbuckle, K. C., Duffel, M. W., Bergman, Å., & Robertson, L. W. (2015). Metabolism and metabolites of polychlorinated biphenyls. Critical Reviews in Toxicology, 45(3), 245–272.
Halkin, B. M., & Filipova, T. O. (2020). Biotransformacija ksenobiotikov mikrobiotoj zheludochno-kishechnogo trakta i ejo posledstvija dlia cheloveka [Biotransformation of the xenobiotics by microbiota of the gastrointestinal tract and its consequences for humans]. Microbiology and Biotechnology, 49, 6–23 (in Russian).
Koppel, N., Maini Rekdal, V., & Balskus, E. P. (2017). Chemical transformation of xenobiotics by the human gut microbiota. Science, 356(6344), eaag2770.
Kozak, V. M., Romanenko, E. R., & Brygadyrenko, V. V. (2020). Influence of herbicides, insecticides and fungicides on food consumption and body weight of Rossiulus kessleri (Diplopoda, Julidae). Biosystems Diversity, 28(3), 272–280.
Kulma, M., Kouřimská, L., Homolková, D., Božik, M., Plachý, V., & Vrabec, V. (2020). Effect of developmental stage on the nutritional value of edible insects. A case study with Blaberus craniifer and Zophobas morio. Journal of Food Composition and Analysis, 92, 103570.
Lambiase, S., Rasola, M., & Grigolo, A. (2004). Daily rhythm, ATP concentration and oxidative activity in an aposymbiotic strain of Blaberus craniifer Burmeister (Blattaria, Blaberidae). Italian Journal of Zoology, 71(4), 305–308.
Lange, C. E., & Lord, J. C. (2012). Chapter. 10. Protistan entomopathogens. In: Vega, F. E., & Kaya, H. K. (Eds.). Insect pathology. Second edition. Academic Press, Amsterdam. Pp. 367–394.
Lieshchova, M. A., Bilan, M. V., Bohomaz, A. A., Tishkina, N. M., & Brygadyrenko, V. V. (2020). Effect of succinic acid on the organism of mice and their intestinal microbiota against the background of excessive fat consumption. Regulatory Mechanisms in Biosystems, 11(2), 153–161.
Lieshchova, M. A., Tishkina, N. M., Bohomaz, A. A., Gavrilin, P. M., & Brygadyrenko, V. V. (2018). Combined effect of glyphosphate, saccharin and sodium benzoate on rats. Regulatory Mechanisms in Biosystems, 9(4), 591–597.
Lieshchova, M., Logvinova, V., Bilan, M., Bohomaz, A., & Brygadyrenko, V. (2023). Effect of azodicarbonamide on rats with a high-fat hypercaloric diet. Acta Fytotechnica et Zootechnica, 26(1), 15–27.
Martynov, V. O., & Brygadyrenko, V. V. (2017). The influence of synthetic food additives and surfactants on the body weight of larvae of Tenebrio molitor (Coleoptera, Tenebrionidae). Biosystems Diversity, 25(3), 236–242.
Martynov, V. O., & Brygadyrenko, V. V. (2018). The influence of the synthetic food colourings tartrazine, allura red and indigo carmine on the body weight of Tenebrio molitor (Coleoptera, Tenebrionidae) larvae. Regulatory Mechanisms in Biosystems, 9(4), 479–484.
Morffe, J., García, N., Véliz, L., Hasegawa, K., & Carreno, R. A. (2022). Morphological and molecular characterization of two species of nematodes (Oxyuridomorpha: Thelastomatoidea: Protrelloididae, Thelastomatidae) parasitic in the cockroach Blaberus discoidalis Serville (Blattaria: Blaberidae) from Cuba. Zootaxa, 5194(1), 92–108.
Parhomenko, O. V., Kolomiichuk, S. V., Omelianov, D. D., & Brygadyrenko, V. V. (2022). Potential use of synthetic and natural aromatic mixtures in prevention from Shelfordella lateralis сockroaches. Regulatory Mechanisms in Biosystems, 13(2), 174–179.
Parhomenko, O. V., Lagutenko, O. T., Lebedynets, N. V., & Brygadyrenko, V. V. (2023). Body-weight gains in Blaberus craniifer cockroaches and the intensity of their infection with gregarines and nematodes. Biosystems Diversity, 31(3), 368–375.
Schecter, A., Colacino, J., Haffner, D., Patel, K., Opel, M., Päpke, O., & Birnbaum, L. (2010). Perfluorinated compounds, polychlorinated biphenyls, and organochlorine pesticide contamination in composite food samples from Dallas, Texas, USA. Environmental Health Perspectives, 118(6), 796–802.
Sender, R., Fuchs, S., & Milo, R. (2016). Revised estimates for the number of human and bacteria cells in the body. PLoS Biology, 14(8), e1002533.
Smith, A. J., & Cook, T. J. (2008). Host specificity of five species of Eugregarinida among six species of cockroaches (Insecta: Blattodea). Comparative Parasitology, 75(2), 288–291.
Tanada, Y., & Kaya, H. K. (1993). Insect pathology. Academic Press, San Diego.
Yanovych, D. O., & Yanovych, N. E. (2011). Biotransformatsija ksenobiotykiv i mekhanizmy yiyi rehulyatsiyi [Biotransformation of xenobiotics and mechanisms of its regulation]. Scientific Bulletin of the LNUVMBT named after S. Z. Gzhitskyi, 48(2), 305–311 (in Ukrainian).
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