Research Article
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Phylogenetic characterization of Cochroaches (Insecta: Blattaria) in Türkiye and determination of their vector potential for medically important parasites

Year 2024, , 417 - 426, 23.09.2024

Fatma Cevahir , Önder Düzlü , Mübeccel Atelge , Alparslan Yıldırım

https://doi.org/10.33988/auvfd.1300194

Abstract

This study was performed to investigate the phylogenetic characters of the cockroaches in the Kayseri region for mitochondrial cytochrome c oxidase subunit I (mt-COI), mt-COII, and internal transcribed spacer-2 (ITS-2) gene regions. It was also aimed to determine their mechanical transmission of medically important parasites. PCR-restriction fragment length polymorphism (RFLP) was performed by using mt-COI, mt-COII, and ITS-2 DNA gene regions to identify cockroach species (n=220) collected from different regions. Differentiation of cockroach species was based on RFLP models using two restriction enzymes: AvaI and EciI. For phylogenetic analysis, mt-COI, mt-COII, and ITS-2 DNA barcode regions were amplified with standard primers. The obtained amplicons were purified and sequenced using the PCR primers. According to PCR-RFLP, the cockroach species were identified as Blattella germanica (n=105), Blatta orientalis (n=86), and Periplaneta americana (n=29). A total of 13 haplotypes were detected and maximum likelihood (ML) analyses revealed that the sequences of all three species showed a monophyletic structure for the three gene regions. The cockroaches were examined for the presence of parasites. It was found that of the 58 parasitic forms identified, 46 (79.3%) belonged to helminth species and 12 (20.7%) to protozoan species. The results showed that B. germanica (58.6%) had the highest prevalence, followed by Bl. orientalis (32.8%) and P. americana (8.6%). The results of the study not only contribute to the molecular epidemiology of cockroaches but also confirm their important role as mechanical vectors of protozoan and helminth parasites.

Keywords

Cockroach DNA barcoding ITS-2 mt‐COI and mt‐COII Vector

Supporting Institution

This study was supported by the Erciyes University Scientific Research Projects Unit with project number TDK-2017-7760.

Project Number

TDK-2017-7760

Thanks

This study was derived from the the first author’s doctoral dissertation.

References

  • Altay K, Dumanlı N (2015): Blattaria. 133-136. In: Karaer Z, Dumanlı N (Eds), Arthropodoloji. Medisan Press, Ankara.
  • Arakere G, Nadig S, Swedberg G, et al (2005): Genotyping of methicillin-resistant Staphylococcus aureus strains from two hospitals in Bangalore, South India. J Clin Microbiol, 43, 3198-3202.
  • Chamavit P, Sahaisook P, Niamnuy N (2011): The majority of cockroaches from the Samutprakarn province of Thailand are carriers of parasitic organisms. EXCLI Journal, 10, 218-222.
  • Chan OT, Lee EK, Hardman JM, et al (2004): The cockroach as a host for Trichinella and Enterobius vermicularis: implications for public health. Hawaii Med J, 63, 74-77.
  • Che Y, Gui S, Lo N, et al (2017): Species delimitation and phylogenetic relationships in ectobiid cockroaches (Dictyoptera, Blattodea) from China. PLoS One, 12, e0169006.
  • Che Y, Wang Z (2013): Three new species of cockroach genus Symploce Hebard, 1916 (Blattodea, Ectobiidae, Blattellinae) with redescriptions of two known species based on types from Mainland China. ZooKeys, 337, 1.
  • Cheng XF, Zhang LP, Yu DN, et al (2016): The complete mitochondrial genomes of four cockroaches (Insecta: Blattodea) and phylogenetic analyses within cockroaches. Gene, 586, 115-122.
  • Cetin H (2015): The importance of vector management for prevention of hospital infections. Turkiye Parazitol Derg, 39, 227-230.
  • El-Sherbini GT, El-Sherbini ET (2011): The role of cockroaches and flies in mechanical transmission of medical important parasites. J Entomol Nematol, 3, 98-104.
  • El-Sherbini GT, Gneidy MR (2012): Cockroaches and flies in mechanical transmission of medical important parasites in Khaldyia Village, El-Fayoum, Governorate, Egypt. J Egypt Soc Parasitol, 240, 1-10.
  • Evangelista D, Buss L, Ware JL (2013): Using DNA barcodes to confirm the presence of a new invasive cockroach pest in New York City. J Econ Entomol, 106, 2275-2279.
  • Evangelista DA, Bourne G, Ware JL (2014): Species richness estimates of B lattodea ss (Insecta: Dictyoptera) from northern G uyana vary depending upon methods of species delimitation. Syst Entomol, 39, 150-158.
  • Everaerts C, Maekawa K, Farine JP, et al (2008): The Cryptocercus punctulatus species complex (Dictyoptera: Cryptocercidae) in the eastern United States: comparison of cuticular hydrocarbons, chromosome number, and DNA sequences. Mol Phylogenet Evol, 47, 950-959.
  • Farmani M, Basseri H, Norouzi B, et al (2019): Ribosomal DNA internal transcribed spacer 2 sequence analysis and phylogenetic comparison of seven cockroach species in northwestern Iran. BMC Res Notes, 12, 1-5.
  • Fathpour H, Emtiazi G, Ghasemi E (2003): Cockroaches as reservoirs and vectors of drug resistant Salmonella spp. Iran Biomed J, 7, 35-38.
  • Fisk FW (1982): Abundance and diversity of arboreal Blattaria in moist tropical forests of the Panama canal area and Costa Rica. T Am Entomol, 479-489.
  • Folmer O, Black M, Hoeh W, et al (1994): DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol, 3, 294-299.
  • Galdiero E, Villari P, Onofrio V, et al (2005): Characterization of glycopeptide resistant enterococci isolated from a hospital in Naples (Italy). New Microbiol, 28, 171-176.
  • Gazeta GS, Freire ML, Ezequiel OS, et al (2007): Artrópodes capturados em ambiente hospitalar do Rio de Janeiro, Brasil. Rev Patol Trop, 36, 254-264.
  • Gliniewicz A, Sawicka B, Czajka E (2003): Occurrence of insect pests in hospitals in Poland. Przegl Epidemiol, 57, 329-334.
  • Guindon S, Gascuel O (2003): A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol, 52, 696-704.
  • Hamu H, Debalke S, Zemene E, et al (2014): Isolation of intestinal parasites of public health importance from cockroaches (Blattella germanica) in Jimma Town, Southwestern Ethiopia. J Parasitol Res, 186240, 1-5.
  • Hristov GH, Chobanov DP (2016). An annotated checklist and key to the Bulgarian cockroaches (Dictyoptera: Blattodea). Zootaxa, 4154, 351-388.
  • Hashemi-Aghdam SS, Rafie G, Akbari S, et al (2017): Utility of mtDNA-COI barcode region for phylogenetic relationship and diagnosis of five common pest cockroaches. J Arthropod-Borne Dis, 11, 182-193.
  • Huelsenbeck JP, Ronquist F (2001): MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754-755.
  • Jarujareet W, Kobayashi M, Taira K, et al (2019): The role of the American cockroach (Periplaneta americana) as transport host of Eimeria tenella to chickens. Parasitol Res, 118, 2311-2315.
  • Kearse M, Moir R, Wilson A, et al (2012): Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647-1649.
  • Kimura M (1980): A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol, 16, 111-120.
  • Knebelsberger T, Miller MA (2007): Revision and phylogeny of the subaptera-group of Phyllodromica (Blattoptera: Blattellidae: Ectobiinae), including a parthenogenetic species and the evaluation of COI sequences for species identification (DNA barcoding). Zootaxa, 1522, 1-68.
  • Kutrup B (2003): Cockroach infestation in some hospitals in Trabzon, Turkey. Turk J Zool, 27, 73-77.
  • Lamiaa B, Lebbadi M, Ahmed A (2007): Bacteriological analysis of Periplaneta americana L. (Dictyoptera; Blattidae) and Musca domestica L. (Diptera; Muscidae) in ten districts of Tangier, Morocco. Afr J Biotechnol, 6, 2038-2042.
  • Librado P, Rozas J (2009): DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
  • Miranda RA, Silva JP (2008): Enterobactérias isoladas de Periplaneta americana capturadas em um ambiente hospitalar. Ciência et Praxis, 1, 21-24.
  • Moges F, Eshetie S, Endris M, et al (2016): Cockroaches as a source of high bacterial pathogens with multidrug resistant strains in Gondar town, Ethiopia. Biomed Res Int, 1-6.
  • Mukha D, Wiegmann BM, Schal C (2002): Evolution and phylogenetic information content of the ribosomal DNA repeat unit in the Blattodea (Insecta). Ins Biochem Mol Biol, 32, 951-960.
  • Nei M, Kumar S (2000): Molecular evolution and phylogenetics: Oxford University Press, USA.
  • Oguz B, Ozdal N, Orunc Kilinc O, et al (2017): First investigation on vectorial potential of Blattella germanica in Turkey. Ankara Univ Vet Fak Derg, 64, 141-144.
  • Park YC, Maekawa K, Matsumoto T, et al (2004): Molecular phylogeny and biogeography of the Korean woodroaches Cryptocercus spp. Mol Phylogenet Evol, 30, 450-464.
  • Pongsiri MJ, Roman J (2007): Examining the links between biodiversity and human health: an interdisciplinary research initiative at the US Environmental Protection Agency. EcoHealth, 4, 82-85.
  • Posada D (2008): jModelTest: phylogenetic model averaging. Mol Biol Evol, 25, 1253-1256.
  • Salehzadeh A, Tavacol P, Mahjub H (2007): Bacterial, fungal and parasitic contamination of cockroaches in public hospitals of Hamadan, Iran. J Vect Borne Dis, 44, 105-110.
  • Sharawi ES, Mahyoub JA, Assagaf AI (2021): Morphological and molecular identification of the American cockroaches (Periplaneta americana)in Jeddah province (Dictyoptera: Blattidae). Int J Entomol Res, 6, 31-36.
  • Sulaiman IM, Anderson M, Khristova M, et al (2011): Development of a PCR–Restriction Fragment Length Polymorphism Protocol for Rapid Detection and Differentiation of Four Cockroach Vectors (Group I “Dirty 22” Species) Responsible for Food Contamination and Spreading of Foodborne Pathogens: Public Health Importance. J Food Prot, 74, 1883-1890.
  • Sulaiman IM, Jacobs E, Simpson S, et al (2017): Identification of 18 vector species belonging to Group I, Group II, and Group III ‘Dirty 22’species known to contaminate food and spread foodborne pathogens: DNA barcoding study of public health importance. Int J Trop Insect Sci, 37, 1-10.
  • Tachbele E, Erku W, Gebre-Michael T, et al (2006): Cockroach-associated food-borne bacterial pathogens from some hospitals and restaurants in Addis Ababa, Ethiopia: Distribution and antibiograms. JRTPH, 5, 34-41.
  • Tamura K, Stecher G, Peterson D, et al (2013): MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol, 30, 2725-2729.
  • Tatfeng YM, Usuanlele MU, Orukpe A, et al (2005): Mechanical transmission of pathogenic organisms: the role of cockroaches. J Vect Borne Dis, 42, 129-134.
  • Wang ZQ, Li Y, Che YL, et al (2015): The wood-feeding genus Cryptocercus (Blattodea: Cryptocercidae), with description of two new species based on female genitalia. Fla Entomol, 98, 260-271.
  • Yılmaz YB, Tunaz H (2013): Bazı bitki uçucu yağlarının ve monoterpenoid bileşenlerinin Amerikan hamambceği, Periplaneta americana (Dictyoptera: Blattidae), erginlerine karşı fumigant toksisitesi. Turk Entomol Derg, 37, 319-328.
  • Yue Q, Wu K, Qiu D, et al (2014): A formal re-description of the cockroach Hebardina concinna anchored on DNA barcodes confirms wing polymorphism and identifies morphological characters for field identification. PLoS One, 9, e106789.
  • Zheng Y, Wang C, Che Y, et al (2016): The species of Symplocodes Hebard (Blattodea: Ectobiidae: Blattellinae) with description of a new species from China. Ann Mag Nat Hist, 50, 339-361.

Year 2024, , 417 - 426, 23.09.2024

Fatma Cevahir , Önder Düzlü , Mübeccel Atelge , Alparslan Yıldırım

https://doi.org/10.33988/auvfd.1300194

Abstract

Supporting Institution

Erciyes Üniversitesi Bilimsel Araştırma Projeleri Birimi

Project Number

TDK-2017-7760

References

  • Altay K, Dumanlı N (2015): Blattaria. 133-136. In: Karaer Z, Dumanlı N (Eds), Arthropodoloji. Medisan Press, Ankara.
  • Arakere G, Nadig S, Swedberg G, et al (2005): Genotyping of methicillin-resistant Staphylococcus aureus strains from two hospitals in Bangalore, South India. J Clin Microbiol, 43, 3198-3202.
  • Chamavit P, Sahaisook P, Niamnuy N (2011): The majority of cockroaches from the Samutprakarn province of Thailand are carriers of parasitic organisms. EXCLI Journal, 10, 218-222.
  • Chan OT, Lee EK, Hardman JM, et al (2004): The cockroach as a host for Trichinella and Enterobius vermicularis: implications for public health. Hawaii Med J, 63, 74-77.
  • Che Y, Gui S, Lo N, et al (2017): Species delimitation and phylogenetic relationships in ectobiid cockroaches (Dictyoptera, Blattodea) from China. PLoS One, 12, e0169006.
  • Che Y, Wang Z (2013): Three new species of cockroach genus Symploce Hebard, 1916 (Blattodea, Ectobiidae, Blattellinae) with redescriptions of two known species based on types from Mainland China. ZooKeys, 337, 1.
  • Cheng XF, Zhang LP, Yu DN, et al (2016): The complete mitochondrial genomes of four cockroaches (Insecta: Blattodea) and phylogenetic analyses within cockroaches. Gene, 586, 115-122.
  • Cetin H (2015): The importance of vector management for prevention of hospital infections. Turkiye Parazitol Derg, 39, 227-230.
  • El-Sherbini GT, El-Sherbini ET (2011): The role of cockroaches and flies in mechanical transmission of medical important parasites. J Entomol Nematol, 3, 98-104.
  • El-Sherbini GT, Gneidy MR (2012): Cockroaches and flies in mechanical transmission of medical important parasites in Khaldyia Village, El-Fayoum, Governorate, Egypt. J Egypt Soc Parasitol, 240, 1-10.
  • Evangelista D, Buss L, Ware JL (2013): Using DNA barcodes to confirm the presence of a new invasive cockroach pest in New York City. J Econ Entomol, 106, 2275-2279.
  • Evangelista DA, Bourne G, Ware JL (2014): Species richness estimates of B lattodea ss (Insecta: Dictyoptera) from northern G uyana vary depending upon methods of species delimitation. Syst Entomol, 39, 150-158.
  • Everaerts C, Maekawa K, Farine JP, et al (2008): The Cryptocercus punctulatus species complex (Dictyoptera: Cryptocercidae) in the eastern United States: comparison of cuticular hydrocarbons, chromosome number, and DNA sequences. Mol Phylogenet Evol, 47, 950-959.
  • Farmani M, Basseri H, Norouzi B, et al (2019): Ribosomal DNA internal transcribed spacer 2 sequence analysis and phylogenetic comparison of seven cockroach species in northwestern Iran. BMC Res Notes, 12, 1-5.
  • Fathpour H, Emtiazi G, Ghasemi E (2003): Cockroaches as reservoirs and vectors of drug resistant Salmonella spp. Iran Biomed J, 7, 35-38.
  • Fisk FW (1982): Abundance and diversity of arboreal Blattaria in moist tropical forests of the Panama canal area and Costa Rica. T Am Entomol, 479-489.
  • Folmer O, Black M, Hoeh W, et al (1994): DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol, 3, 294-299.
  • Galdiero E, Villari P, Onofrio V, et al (2005): Characterization of glycopeptide resistant enterococci isolated from a hospital in Naples (Italy). New Microbiol, 28, 171-176.
  • Gazeta GS, Freire ML, Ezequiel OS, et al (2007): Artrópodes capturados em ambiente hospitalar do Rio de Janeiro, Brasil. Rev Patol Trop, 36, 254-264.
  • Gliniewicz A, Sawicka B, Czajka E (2003): Occurrence of insect pests in hospitals in Poland. Przegl Epidemiol, 57, 329-334.
  • Guindon S, Gascuel O (2003): A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol, 52, 696-704.
  • Hamu H, Debalke S, Zemene E, et al (2014): Isolation of intestinal parasites of public health importance from cockroaches (Blattella germanica) in Jimma Town, Southwestern Ethiopia. J Parasitol Res, 186240, 1-5.
  • Hristov GH, Chobanov DP (2016). An annotated checklist and key to the Bulgarian cockroaches (Dictyoptera: Blattodea). Zootaxa, 4154, 351-388.
  • Hashemi-Aghdam SS, Rafie G, Akbari S, et al (2017): Utility of mtDNA-COI barcode region for phylogenetic relationship and diagnosis of five common pest cockroaches. J Arthropod-Borne Dis, 11, 182-193.
  • Huelsenbeck JP, Ronquist F (2001): MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754-755.
  • Jarujareet W, Kobayashi M, Taira K, et al (2019): The role of the American cockroach (Periplaneta americana) as transport host of Eimeria tenella to chickens. Parasitol Res, 118, 2311-2315.
  • Kearse M, Moir R, Wilson A, et al (2012): Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647-1649.
  • Kimura M (1980): A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol, 16, 111-120.
  • Knebelsberger T, Miller MA (2007): Revision and phylogeny of the subaptera-group of Phyllodromica (Blattoptera: Blattellidae: Ectobiinae), including a parthenogenetic species and the evaluation of COI sequences for species identification (DNA barcoding). Zootaxa, 1522, 1-68.
  • Kutrup B (2003): Cockroach infestation in some hospitals in Trabzon, Turkey. Turk J Zool, 27, 73-77.
  • Lamiaa B, Lebbadi M, Ahmed A (2007): Bacteriological analysis of Periplaneta americana L. (Dictyoptera; Blattidae) and Musca domestica L. (Diptera; Muscidae) in ten districts of Tangier, Morocco. Afr J Biotechnol, 6, 2038-2042.
  • Librado P, Rozas J (2009): DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
  • Miranda RA, Silva JP (2008): Enterobactérias isoladas de Periplaneta americana capturadas em um ambiente hospitalar. Ciência et Praxis, 1, 21-24.
  • Moges F, Eshetie S, Endris M, et al (2016): Cockroaches as a source of high bacterial pathogens with multidrug resistant strains in Gondar town, Ethiopia. Biomed Res Int, 1-6.
  • Mukha D, Wiegmann BM, Schal C (2002): Evolution and phylogenetic information content of the ribosomal DNA repeat unit in the Blattodea (Insecta). Ins Biochem Mol Biol, 32, 951-960.
  • Nei M, Kumar S (2000): Molecular evolution and phylogenetics: Oxford University Press, USA.
  • Oguz B, Ozdal N, Orunc Kilinc O, et al (2017): First investigation on vectorial potential of Blattella germanica in Turkey. Ankara Univ Vet Fak Derg, 64, 141-144.
  • Park YC, Maekawa K, Matsumoto T, et al (2004): Molecular phylogeny and biogeography of the Korean woodroaches Cryptocercus spp. Mol Phylogenet Evol, 30, 450-464.
  • Pongsiri MJ, Roman J (2007): Examining the links between biodiversity and human health: an interdisciplinary research initiative at the US Environmental Protection Agency. EcoHealth, 4, 82-85.
  • Posada D (2008): jModelTest: phylogenetic model averaging. Mol Biol Evol, 25, 1253-1256.
  • Salehzadeh A, Tavacol P, Mahjub H (2007): Bacterial, fungal and parasitic contamination of cockroaches in public hospitals of Hamadan, Iran. J Vect Borne Dis, 44, 105-110.
  • Sharawi ES, Mahyoub JA, Assagaf AI (2021): Morphological and molecular identification of the American cockroaches (Periplaneta americana)in Jeddah province (Dictyoptera: Blattidae). Int J Entomol Res, 6, 31-36.
  • Sulaiman IM, Anderson M, Khristova M, et al (2011): Development of a PCR–Restriction Fragment Length Polymorphism Protocol for Rapid Detection and Differentiation of Four Cockroach Vectors (Group I “Dirty 22” Species) Responsible for Food Contamination and Spreading of Foodborne Pathogens: Public Health Importance. J Food Prot, 74, 1883-1890.
  • Sulaiman IM, Jacobs E, Simpson S, et al (2017): Identification of 18 vector species belonging to Group I, Group II, and Group III ‘Dirty 22’species known to contaminate food and spread foodborne pathogens: DNA barcoding study of public health importance. Int J Trop Insect Sci, 37, 1-10.
  • Tachbele E, Erku W, Gebre-Michael T, et al (2006): Cockroach-associated food-borne bacterial pathogens from some hospitals and restaurants in Addis Ababa, Ethiopia: Distribution and antibiograms. JRTPH, 5, 34-41.
  • Tamura K, Stecher G, Peterson D, et al (2013): MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol, 30, 2725-2729.
  • Tatfeng YM, Usuanlele MU, Orukpe A, et al (2005): Mechanical transmission of pathogenic organisms: the role of cockroaches. J Vect Borne Dis, 42, 129-134.
  • Wang ZQ, Li Y, Che YL, et al (2015): The wood-feeding genus Cryptocercus (Blattodea: Cryptocercidae), with description of two new species based on female genitalia. Fla Entomol, 98, 260-271.
  • Yılmaz YB, Tunaz H (2013): Bazı bitki uçucu yağlarının ve monoterpenoid bileşenlerinin Amerikan hamambceği, Periplaneta americana (Dictyoptera: Blattidae), erginlerine karşı fumigant toksisitesi. Turk Entomol Derg, 37, 319-328.
  • Yue Q, Wu K, Qiu D, et al (2014): A formal re-description of the cockroach Hebardina concinna anchored on DNA barcodes confirms wing polymorphism and identifies morphological characters for field identification. PLoS One, 9, e106789.
  • Zheng Y, Wang C, Che Y, et al (2016): The species of Symplocodes Hebard (Blattodea: Ectobiidae: Blattellinae) with description of a new species from China. Ann Mag Nat Hist, 50, 339-361.
There are 51 citations in total.

Details

Primary Language English
Subjects Veterinary Parasitology
Journal Section Research Article
Authors

Fatma Cevahir 0000-0002-4834-5046

Önder Düzlü 0000-0002-6951-0901

Mübeccel Atelge 0000-0003-3019-7038

Alparslan Yıldırım 0000-0001-9868-0363

Project Number TDK-2017-7760
Early Pub Date March 19, 2024
Publication Date September 23, 2024
Published in Issue Year 2024

Cite

APA Cevahir, F., Düzlü, Ö., Atelge, M., Yıldırım, A. (2024). Phylogenetic characterization of Cochroaches (Insecta: Blattaria) in Türkiye and determination of their vector potential for medically important parasites. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 71(4), 417-426. https://doi.org/10.33988/auvfd.1300194
AMA Cevahir F, Düzlü Ö, Atelge M, Yıldırım A. Phylogenetic characterization of Cochroaches (Insecta: Blattaria) in Türkiye and determination of their vector potential for medically important parasites. Ankara Univ Vet Fak Derg. September 2024;71(4):417-426. doi:10.33988/auvfd.1300194
Chicago Cevahir, Fatma, Önder Düzlü, Mübeccel Atelge, and Alparslan Yıldırım. “Phylogenetic Characterization of Cochroaches (Insecta: Blattaria) in Türkiye and Determination of Their Vector Potential for Medically Important Parasites”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71, no. 4 (September 2024): 417-26. https://doi.org/10.33988/auvfd.1300194.
EndNote Cevahir F, Düzlü Ö, Atelge M, Yıldırım A (September 1, 2024) Phylogenetic characterization of Cochroaches (Insecta: Blattaria) in Türkiye and determination of their vector potential for medically important parasites. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71 4 417–426.
IEEE F. Cevahir, Ö. Düzlü, M. Atelge, and A. Yıldırım, “Phylogenetic characterization of Cochroaches (Insecta: Blattaria) in Türkiye and determination of their vector potential for medically important parasites”, Ankara Univ Vet Fak Derg, vol. 71, no. 4, pp. 417–426, 2024, doi: 10.33988/auvfd.1300194.
ISNAD Cevahir, Fatma et al. “Phylogenetic Characterization of Cochroaches (Insecta: Blattaria) in Türkiye and Determination of Their Vector Potential for Medically Important Parasites”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71/4 (September 2024), 417-426. https://doi.org/10.33988/auvfd.1300194.
JAMA Cevahir F, Düzlü Ö, Atelge M, Yıldırım A. Phylogenetic characterization of Cochroaches (Insecta: Blattaria) in Türkiye and determination of their vector potential for medically important parasites. Ankara Univ Vet Fak Derg. 2024;71:417–426.
MLA Cevahir, Fatma et al. “Phylogenetic Characterization of Cochroaches (Insecta: Blattaria) in Türkiye and Determination of Their Vector Potential for Medically Important Parasites”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 71, no. 4, 2024, pp. 417-26, doi:10.33988/auvfd.1300194.
Vancouver Cevahir F, Düzlü Ö, Atelge M, Yıldırım A. Phylogenetic characterization of Cochroaches (Insecta: Blattaria) in Türkiye and determination of their vector potential for medically important parasites. Ankara Univ Vet Fak Derg. 2024;71(4):417-26.