Trypanosomes of the Trypanosoma theileri Group: Phylogeny and New Potential Vectors
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
251477
Grant Agency of Charles University
PubMed
35208749
PubMed Central
PMC8880487
DOI
10.3390/microorganisms10020294
PII: microorganisms10020294
Knihovny.cz E-zdroje
- Klíčová slova
- Phlebotomus, Trypanosoma melophagium, Trypanosoma theileri, ked, mosquito, phylogeny, prediuresis, tabanid, transmission, vector,
- Publikační typ
- časopisecké články MeSH
Trypanosomes belonging to Trypanosoma theileri group are mammalian blood parasites with keds and horse fly vectors. Our aim is to study to vector specificity of T. theileri trypanosomes. During our bloodsucking Diptera survey, we found a surprisingly high prevalence of T. theileri trypanosomes in mosquitoes (154/4051). Using PCR and gut dissections, we detected trypanosomes of T. theileri group mainly in Aedes mosquitoes, with the highest prevalence in Ae. excrucians (22%), Ae. punctor (21%), and Ae. cantans/annulipes (10%). Moreover, T. theileri group were found in keds and blackflies, which were reported as potential vectors for the first time. The vectorial capacity was confirmed by experimental infections of Ae. aegypti using our isolates from mosquitoes; sand fly Phlebotomus perniciosus supported the development of trypanosomes as well. Infection rates were high in both vectors (47-91% in mosquitoes, 65% in sandflies). Furthermore, metacyclic stages of T. theileri trypanosomes were observed in the gut of infected vectors; these putative infectious forms were found in the urine of Ae. aegypti after a second bloodmeal. On the contrary, Culex pipiens quinquefasciatus was refractory to experimental infections. According to a phylogenetic analysis of the 18S rRNA gene, our trypanosomes belong into three lineages, TthI, ThII, and a lineage referred to as here a putative lineage TthIII. The TthI lineage is transmitted by Brachycera, while TthII and ThIII include trypanosomes from Nematocera. In conclusion, we show that T. theileri trypanosomes have a wide range of potential dipteran vectors, and mosquitoes and, possibly, sandflies serve as important vectors.
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Adl S.M., Bass D., Lane C.E., Lukeš J., Schoch C.L., Smirnov A., Agatha S., Berney C., Brown M.W., Burki F., et al. Revisions to the Classification, Nomenclature, and Diversity of Eukaryotes. J. Eukaryot. Microbiol. 2019;66:4–119. doi: 10.1111/jeu.12691. PubMed DOI PMC
Hoare C.A. The Trypanosomes of Mammals: Zoological Monograph. Blackwell Scientific Publications; Oxford, UK: 1972.
Rodrigues A.C., Campaner M., Takata C.S.A., Dell’ Porto A., Milder R.V., Takeda G.F., Teixeira M.M.G. Brazilian isolates of Trypanosoma (Megatrypanum) theileri: Diagnosis and differentiation of isolates from cattle and water buffalo based on biological characteristics and randomly amplified DNA sequences. Vet. Parasitol. 2003;116:185–207. doi: 10.1016/S0304-4017(03)00236-X. PubMed DOI
Kingston N., Morton J.K. Trypanosoma cervi sp. n. from elk (Cervus canadensis) in Wyoming. J. Parasitol. 1975;61:17–23. doi: 10.2307/3279099. PubMed DOI
Kingston N., Bobek B., Perzanowski K., Wita I., Maki L. Description of Trypanosoma (Megatrypanum) stefanskii sp. n. from roe deer (Capreolus capreolus) in Poland. J. Helminthol. Soc. 1992;59:89–95.
Garcia H.A., Blanco P.A., Rodrigues A.C., Rodrigues C.M.F., Takata C.S.A., Campaner M., Camargo E.P., Teixeira M.M.G. Pan-american Trypanosoma (Megatrypanum) trinaperronei n. sp. in the white-tailed deer Odocoileus virginianus Zimmermann and its deer ked Lipoptena mazamae Rondani, 1878: Morphological, developmental and phylogeographical characterisation. Parasit. Vectors. 2020;13:308. doi: 10.1186/s13071-020-04169-0. PubMed DOI PMC
Suganuma K., Kondoh D., Sivakumar T., Mizushima D., Elata A.T.M., Thekisoe O.M.M., Yokoyama N., Inoue N. Molecular characterization of a new Trypanosoma (Megatrypanum) theileri isolate supports the two main phylogenetic lineages of this species in Japanese cattle. Parasitol. Res. 2019;118:1927–1935. doi: 10.1007/s00436-019-06313-x. PubMed DOI
Wells E.A. Subgenus Megatrypanum. In: Lumsden W.H.R., Evans D.A., editors. Biology of the Kinetoplastida. Volume 1. Academic Press; Cambridge, MA, USA: 1976. pp. 257–284.
Doherty M.L., Windle H., Voorheis H.P., Larkin H., Casey M., Clery D., Murray M. Clinical disease associated with Trypanosoma theileri infection in a calf in Ireland. Vet. Rec. 1993;132:653–656. doi: 10.1136/vr.132.26.653. PubMed DOI
Seifi H.A. Clinical trypanosomosis due to Trypanosoma theileri in a cow in Iran. Trop. Anim. Health Prod. 1995;27:93–94. doi: 10.1007/BF02236319. PubMed DOI
Greco A., Loria G.R., Dara S., Luckins T., Sparagano O. First isolation of Trypanosoma theileri in sicilian cattle. Vet. Res. Commun. 2000;24:471–475. doi: 10.1023/A:1006403706224. PubMed DOI
Braun U., Rogg E., Walser M., Nehrbass D., Guscetti F., Mathis A., Deplazes P. Trypanosoma theileri in the cerebrospinal fluid and brain of a heifer with suppurative meningoencephalitis. Vet. Rec. 2002;150:18–19. doi: 10.1136/vr.150.1.18. PubMed DOI
Sood N.K., Singla L.D., Singh R.S., Uppal S.K. Association of Trypanosoma theileri with peritonitis in a pregnant cross-bred cow: A case report. Vet. Med. 2011;56:82–84. doi: 10.17221/1580-VETMED. DOI
Hajihassani A., Maroufi S., Esmaeilnejad B., Khorram H., Tavassoli M., Dalir-Naghadeh B., Samiei A. Hemolytic anemia associated with Trypanosoma theileri in a cow from Kurdistan province, West of Iran. Vet. Res. Forum. 2020;11:191–193. doi: 10.30466/vrf.2019.103834.2465. PubMed DOI PMC
Bittner L., Krämer K., Wöckel A., Snedec T., Delling C., Böttcher D., Köller G., Baumgartner W., Richardt W., Starke A. Malnutrition as the cause of recumbency in suckler cows associated with Trypanosoma theileri infection. Acta Vet. Scand. 2021;63:1–8. doi: 10.1186/s13028-020-00567-7. PubMed DOI PMC
Rodrigues A.C., Paiva F., Campaner M., Stevens J.R., Noyes H.A., Teixeira M.M.G. Phylogeny of Trypanosoma (Megatrypanum) theileri and related trypanosomes reveals lineages of isolates associated with artiodactyl hosts diverging on SSU and ITS ribosomal sequences. Parasitology. 2006;132:215–224. doi: 10.1017/S0031182005008929. PubMed DOI
Garcia H.A., Rodrigues A.C., Martinkovic F., Minervino A.H.H., Campaner M., Nunes V.L.B., Paiva F., Hamilton P.B., Teixeira M.M.G. Multilocus phylogeographical analysis of Trypanosoma (Megatrypanum) genotypes from sympatric cattle and water buffalo populations supports evolutionary host constraint and close phylogenetic relationships with genotypes found in other ruminants. Int. J. Parasitol. 2011;41:1385–1396. doi: 10.1016/j.ijpara.2011.09.001. PubMed DOI
Yokoyama N., Sivakumar T., Fukushi S., Tattiyapong M., Tuvshintulga B., Kothalawala H., Silva S.S.P., Igarashi I., Inoue N. Genetic diversity in Trypanosoma theileri from Sri Lankan cattle and water buffaloes. Vet. Parasitol. 2015;207:335–341. doi: 10.1016/j.vetpar.2014.12.006. PubMed DOI
Pacheco M.A., Cepeda A.S., Bernotienė R., Lotta I.A., Matta N.E., Valkiūnas G., Escalante A.A. Primers targeting mitochondrial genes of avian haemosporidians: PCR detection and differential DNA amplification of parasites belonging to different genera. Int. J. Parasitol. 2018;48:657–670. doi: 10.1016/j.ijpara.2018.02.003. PubMed DOI PMC
Gibson W., Pilkington J.G., Pemberton J.M. Trypanosoma melophagium from the sheep ked Melophagus ovinus on the island of St Kilda. Parasitology. 2010;137:1799–1804. doi: 10.1017/S0031182010000752. PubMed DOI
Martinković F., Matanović K., Rodrigues A.C., Garcia H.A., Teixeira M.M.G. Trypanosoma (Megatrypanum) melophagium in the sheep ked Melophagus ovinus from organic farms in Croatia: Phylogenetic inferences support restriction to sheep and sheep keds and close relationship with trypanosomes from other ruminant species. J. Eukaryot. Microbiol. 2012;59:134–144. doi: 10.1111/j.1550-7408.2011.00599.x. PubMed DOI
Fisher A.C., Schuster G., Cobb W.J., James A.M., Cooper S.M., Peréz de León A.A., Holman P.J. Molecular characterization of Trypanosoma (Megatrypanum) spp. infecting cattle (Bos taurus), white-tailed deer (Odocoileus virginianus), and elk (Cervus elaphus canadensis) in the United States. Vet. Parasitol. 2013;197:29–42. doi: 10.1016/j.vetpar.2013.04.037. PubMed DOI
Böse R., Friedhoff K.T., Olbrich S. Transmission of Megatrypanum Trypanosomes to Cervus dama by Tabanidae. J. Protozool. 1987;34:110–113. doi: 10.1111/j.1550-7408.1987.tb03143.x. PubMed DOI
Böhm M., White P.C.L., Chambers J., Smith L., Hutchings M.R. Wild deer as a source of infection for livestock and humans in the UK. Vet. J. 2007;174:260–276. doi: 10.1016/j.tvjl.2006.11.003. PubMed DOI
Kingston N., Thorne E.T., Thomas G.M., McHolland L., Trueblood M.S. Further studies on trypanosomes in game animals in Wyoming II. J. Wildl. Dis. 1981;17:539–546. doi: 10.7589/0090-3558-17.4.539. PubMed DOI
Lanevschi-Pietersma A., Ogunremi O., Desrochers A. Parasitemia in a neonatal bison calf. Vet. Clin. Pathol. 2004;33:173–176. doi: 10.1111/j.1939-165X.2004.tb00370.x. PubMed DOI
Nijhout H.F., Grant M.C. Diuresis after a bloodmeal in female Anopheles freeborni. J. Insect Physiol. 1978;24:293–298. doi: 10.1016/0022-1910(78)90025-2. DOI
Briegel H., Rezzonico L. Concentration of host blood protein during feeding by anopheline mosquitoes (Diptera: Culicidae) J. Med. Entomol. 1985;22:612–618. doi: 10.1093/jmedent/22.6.612. PubMed DOI
Maddrell S.H. Excretion in the blood-sucking bug, Rhodnius prolixus Stal. I. The control of diuresis. J. Exp. Biol. 1964;41:163–176. doi: 10.1242/jeb.41.1.163. PubMed DOI
Gee J.D. The control of diuresis in the tsetse fly Glossina austeni: A preliminary investigation of the diuretic hormone. J. Exp. Biol. 1975;63:391–401. doi: 10.1242/jeb.63.2.391. PubMed DOI
Jones J.C., Brandt E. Fluid excretion by adult Aedes aegypti mosquitoes. J. Insect Physiol. 1981;27:545–549. doi: 10.1016/0022-1910(81)90042-1. DOI
Sádlová J., Reishig J., Volf P. Prediuresis in female Phlebotomus sandflies (Diptera: Psychodidae) Eur. J. Entomol. 1998;95:643–647.
Fialová M., Santolíková A., Brotánková A., Brzoňová J., Svobodová M. Complete Life Cycle of Trypanosoma thomasbancrofti, an Avian Trypanosome Transmitted by Culicine Mosquitoes. Microorganisms. 2021;9:2101. doi: 10.3390/microorganisms9102101. PubMed DOI PMC
Mutero C.M., Mutinga M.J. Defecation by Anopheles arabiensis mosquitoes of host blood infected with live Trypanosoma congolense. Trop. Med. Parasitol. 1993;44:23–26. PubMed
Sádlová J., Volf P. Occurrence of Leishmania major in sandfly urine. Parasitology. 1999;118:455–460. doi: 10.1017/S0031182099004254. PubMed DOI
Galen S.C., Borner J., Perkins S.L., Weckstein J.D. Phylogenomics from transcriptomic “bycatch” clarify the origins and diversity of avian trypanosomes in North America. PLoS ONE. 2020;15 doi: 10.1371/journal.pone.0240062. PubMed DOI PMC
Böse R., Heister N.C. Development of Trypanosoma (M.) theileri in Tabanids. J. Eukaryot. Microbiol. 1993;40:788–792. doi: 10.1111/j.1550-7408.1993.tb04475.x. PubMed DOI
Ganyukova A.I., Zolotarev A.V., Malysheva M.N., Frolov A.O. First record of Trypanosoma theileri-like flagellates in horseflies from Northwest Russia. Protistology. 2018;12:223–230. doi: 10.21685/1680-0826-2018-12-4-6. DOI
Böse R., Petersen K. Lipoptena cervi (Diptera), a potencial vector of Megatrypanum trypanosomes of deer (Cervidae) Parasitol. Res. 1991;77:723–725. doi: 10.1007/BF00928691. PubMed DOI
Werszko J., Steiner-Bogdaszewska Z., Jeżewski W., Szewczyk T., Kuryło G., Wołkowycki M., Wróblewski P., Karbowiak G. Molecular detection of Trypanosoma spp. in Lipoptena cervi and Lipoptena fortisetosa (Diptera: Hippoboscidae) and their potential role in the transmission of pathogens. Parasitology. 2020;147:1629–1635. doi: 10.1017/S0031182020001584. PubMed DOI PMC
Schoener E., Uebleis S.S., Cuk C., Nawratil M., Obwaller A.G., Zechmeister T., Lebl K., Rádrová J., Zittra C., Votýpka J., et al. Trypanosomatid parasites in Austrian mosquitoes. PLoS ONE. 2018;13:e0141332. doi: 10.1371/journal.pone.0196052. PubMed DOI PMC
Calzolari M., Rugna G., Clementi E., Carra E., Pinna M., Bergamini F., Fabbi M., Dottori M., Sacchi L., Votýpka J. Isolation of a trypanosome related to Trypanosoma theileri (Kinetoplastea: Trypanosomatidae) from Phlebotomus perfiliewi (Diptera: Psychodidae) Biomed. Res. Int. 2018;2018 doi: 10.1155/2018/2597074. PubMed DOI PMC
Votýpka J., Rádrová J., Skalický T., Jirků M., Jirsová D., Mihalca A.D., D’Amico G., Petrželková K.J., Modrý D., Lukeš J. A tsetse and tabanid fly survey of African great apes habitats reveals the presence of a novel trypanosome lineage but the absence of Trypanosoma brucei. Int. J. Parasitol. 2015;45:741–748. doi: 10.1016/j.ijpara.2015.06.005. PubMed DOI
Ngomtcho S.C.H., Weber J.S., Ngo Bum E., Gbem T.T., Kelm S., Achukwi M.D. Molecular screening of tsetse flies and cattle reveal different Trypanosoma species including T. grayi and T. theileri in northern Cameroon. Parasites Vectors. 2017;10:1–16. doi: 10.1186/s13071-017-2540-7. PubMed DOI PMC
Krinsky A.W.L., Burgdorfer W. Trypanosomes in Amblyomma americanum from Oklahoma. J. Parasitol. 1976;62:824–825. doi: 10.2307/3278970. PubMed DOI
Shastri U.V., Deshpande P.D. Hyalomma anatolicum anatolicum (Koch, 1844) as a possible vector for transmission of Trypanosoma theileri, Laveran, 1902 in cattle. Vet. Parasitol. 1981;9:151–155. doi: 10.1016/0304-4017(81)90034-0. PubMed DOI
Latif A.A., Bakheit M.A., Mohamed A.E., Zweygarth E. High infection rates of the tick Hyalomma anatolicum anatolicum with Trypanosoma theileri. Onderstepoort J. Vet. Res. 2004;71:251–256. doi: 10.4102/ojvr.v71i4.228. PubMed DOI
Martins J.R., Leite R.C., Doyle R.L. Tripanosomatides like Trypanosoma theileri in the cattle tick Boophilus microplus. Rev. Bras. Parasitol. Vet. 2008;17:113–114. doi: 10.1590/S1984-29612008000200010. PubMed DOI
Molyneux D.H. Trypanosoma (Megatrypanum) melophagium: Modes of attachment of parasites to mid-gut, hindgut and rectum of the sheep ked, Melophagus ovinus. Acta Trop. 1975;32:65–74. PubMed
Molyneux D.H., Selkirk M., Lavin D. Trypanosoma (Megatrypanum) melophagium in the sheep ked, Melophagus ovinus: A scanning electron microscope (SEM) study of the parasites and the insect gut wall surfaces. Acta Trop. 1978;35:319–328. PubMed
Votýpka J., Szabová J., Rádrová J., Zídková L., Svobodová M. Trypanosoma culicavium sp. nov., an avian trypanosome transmitted by Culex mosquitoes. Int. J. Syst. Evol. Microbiol. 2012;62:745–754. doi: 10.1099/ijs.0.032110-0. PubMed DOI
Rodrigues A.C., Garcia H.A., Batista J.S., Minervino A.H.H., Góes-Cavalcante G., Maia da Silva F., Ferreira R.C., Campaner M., Paiva F., Teixeira M.M.G. Characterization of spliced leader genes of Trypanosoma (Megatrypanum) theileri: Phylogeographical analysis of brazilian isolates from cattle supports spatial clustering of genotypes and parity with ribosomal markers. Parasitology. 2010;137:111–122. doi: 10.1017/S0031182009991053. PubMed DOI
Pacheco T.D.A., Marcili A., da Costa A.P., Witter R., Melo A.L.T., Boas R.V., Chitarra C.S., Dutra V., Nakazato L., de Pacheco R.C. Genetic diversity and molecular survey of Trypanosoma (Megatrypanum) theileri in cattle in Brazil’s western Amazon region. Rev. Bras. Parasitol. Vet. 2018;27:579–583. doi: 10.1590/s1984-296120180049. PubMed DOI
Jaimes-Dueñez J., Triana-Chávez O., Mejía-Jaramillo A.M. Spatial-temporal and phylogeographic characterization of Trypanosoma spp. in cattle (Bos taurus) and buffaloes (Bubalus bubalis) reveals transmission dynamics of these parasites in Colombia. Vet. Parasitol. 2018;249:30–42. doi: 10.1016/j.vetpar.2017.11.004. PubMed DOI
Kramář J. Fauna ČSR, Svazek 13, Komáři Bodaví—Culicinae. Czechoslovak Academy of Sciences; Prague, Czech Republic: 1958.
Chvála M., Hůrka K., Chalupský J., Knoz J., Minář J., Országh I. Fauna ČSR, Svazek 22, Krevsající Mouchy a Střečci. Nakladatelství Československé Akademie Věd; Prague, Czech Republic: 1980. Hippoboscidae—Klošovití; pp. 475–478.
Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 1994;3:294–299. PubMed
Medlin L.K., Elwood H.J., Stickel S., Sogin M.L. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene. 1988;71:491–499. doi: 10.1016/0378-1119(88)90066-2. PubMed DOI
Maslov D.A., Lukeš J., Jirků M., Simpson L. Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: Implications for the evolution of parasitism in the trypanosomatid protozoa. Mol. Biochem. Parasitol. 1996;75:197–205. doi: 10.1016/0166-6851(95)02526-X. PubMed DOI
Santolíková A. Master’s Thesis. Charles University; Prague, Czech Republic: 2019. Role Klošů v Přenosu Ptačích Trypanosom (The Role of Hippoboscids in Avian Trypanosomes Transmission)
Zídková L., Cepicka I., Szabová J., Svobodová M. Biodiversity of avian trypanosomes. Infect. Genet. Evol. 2012;12:102–112. doi: 10.1016/j.meegid.2011.10.022. PubMed DOI
Hlaváčová J., Votýpka J., Volf P. The effect of temperature on Leishmania (Kinetoplastida: Trypanosomatidae) development in sand flies. J. Med. Entomol. 2013;50:955–958. doi: 10.1603/ME13053. PubMed DOI
Rasband W.S. ImageJ. National Institute of Health; Bethesda, MD, USA: 1997.
Katoh K., Misawa K., Kuma K.I., Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl. Acids Res. 2002;30:3059–3066. doi: 10.1093/nar/gkf436. PubMed DOI PMC
Hall T. BioEdit: An important software for molecular biology. GERF Bull. Biosci. 2011;2:60–61. doi: 10.1017/S0317167100012865. DOI
Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC
Böse R., Petersen K., Pospichal H., Buchanan N., Tait A. Characterization of Megatrypanum trypanosomes from European Cervidae. Parasitology. 1993;107:55–61. doi: 10.1017/S0031182000079403. PubMed DOI
Börstler J., Jöst H., Garms R., Krüger A., Tannich E., Becker N., Schmidt-Chanasit J., Lühken R. Host-feeding patterns of mosquito species in Germany. Paras. Vectors. 2016;9:1–14. doi: 10.1186/s13071-016-1597-z. PubMed DOI PMC
Schönenberger A.C., Wagner S., Tuten H.C., Schaffner F., Torgerson P., Furrer S., Mathis A., Silaghi C. Host preferences in host-seeking and blood-fed mosquitoes in Switzerland. Med. Vet. Entomol. 2016;30:39–52. doi: 10.1111/mve.12155. PubMed DOI
Rádrová J., Šeblová V., Votýpka J. Feeding behavior and spatial distribution of Culex mosquitoes (Diptera: Culicidae) in wetland areas of the Czech Republic. J. Med. Entomol. 2013;50:1097–1104. doi: 10.1603/ME13029. PubMed DOI
Small R.W. A review of Melophagus ovinus (L.), the sheep ked. Vet. Parasitol. 2005;130:141–155. doi: 10.1016/j.vetpar.2005.03.005. PubMed DOI
Seblova V., Sadlova J., Carpenter S., Volf P. Development of Leishmania parasites in Culicoides nubeculosus (Diptera: Ceratopogonidae) and implications for screening vector competence. J. Med. Entomol. 2012;49:967–970. doi: 10.1603/ME12053. PubMed DOI
Werszko J., Szewczyk T., Steiner-Bogdaszewska Z., Wróblewski P., Karbowiak G., Laskowski Z. Molecular detection of Megatrypanum trypanosomes in tabanid flies. Med. Vet. Entomol. 2019:1–5. doi: 10.1111/mve.12409. PubMed DOI
Hoffmann M., Buscher G., Friedhoff K.T. Stercorarian trypanosomes from deer (Cervidae) in Germany. J. Protozool. 1984;31:581–584. doi: 10.1111/j.1550-7408.1984.tb05509.x. PubMed DOI
Neumuller M., Nilsson K., Pahlson C. Trypanosoma spp. in Swedish game animals. Parasitol. Res. 2012;110:135–139. doi: 10.1007/s00436-011-2462-9. PubMed DOI
Githeko A.K., Lindsay S.W., Confalonieri U.E., Patz J.A. Climate change and vector-borne diseases: A regional analysis. Bull. World Health Organ. 2000;78:1136–1147. doi: 10.1590/S0042-96862000000900009. PubMed DOI PMC
Gage K.L., Burkot T.R., Eisen R.J., Hayes E.B. Climate and vectorborne diseases. Am. J. Prev. Med. 2008;35:436–450. doi: 10.1016/j.amepre.2008.08.030. PubMed DOI
Reinhold J.M., Lazzari C.R., Lahondère C. Effects of the environmental temperature on Aedes aegypti and Aedes albopictus mosquitoes: A review. Insects. 2018;9:158. doi: 10.3390/insects9040158. PubMed DOI PMC
Galková Z. Master’s Thesis. Charles University; Prague, Czech Republic: 2010. Tiplíci Jako Přenašeči Infekčních Onemocnění a Jejich Výskyt na Území ČR.