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Morphological, molecular and developmental characterization of the thelastomatid nematode Thelastoma bulhoesi (de Magalhães, 1900) (Oxyuridomorpha: Thelastomatidae) parasite of Periplaneta americana (Linnaeus, 1758) (Blattodea: Blattidae) in Japan

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Abstract

The American cockroach Periplaneta americana (Linnaeus, 1758) (Blattodea: Blattidae) has been spreading worldwide by commerce and has successfully adjusted to living with humans. There are many reports of thelastomatid parasitic nematode isolated from P. americana in many countries including USA, Canada, India, Argentina, Bulgaria, but not in Japan. We have investigated the parasitic nematodes in P. americana lab strain and field-captured individuals in Japan and found that Thelastoma bulhoesi (de Magalhães, 1900) (Oxyuridomorpha: Thelastomatidae) parasitizes with high infection rates. We described morphological, molecular, and developmental characters of the parasitic nematode because such information was missing despite it has been discovered more than one hundred years ago. We described morphometrics with DIC microscopy and fine structure of male and female adult with SEM observation. We also reveal the embryonic and postembryonic development of this nematode. This is the first report of a thelastomatid nematode isolated from American cockroach in Japan, and the data showed here is also very useful and fundamental for further analysis of the cockroach and parasite relations.

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References

  • Adamson M.L., Clease D.F. 1989. Morphological changes during in ovo development in the Thelastomatoidea: description and functional considerations. Journal of Parasitology, 75, 728–734

    Article  Google Scholar 

  • Adamson M.L., Noble S.J. 1993. Interspecific and intraspecific competition among pinworms in the hindgut of Periplaneta americana. Journal of Parasitology, 79, 50–56

    Article  Google Scholar 

  • Adamson M.L., Van Waerebeke D. 1992. Revision of the Thelastomatoidea, Oxyurida of invertebrate hosts I. Thelastomatidae. Systematic Parasitology, 21, 21–63

    Article  Google Scholar 

  • Ainsworth R. 1991. Cytogenetic evidence of haplodiploidy in two species of nematode (Pharyngodonidae: Oxyurida) from New Zealand lizards. Journal of Parasitology, 77, 92–98

    Article  Google Scholar 

  • Appel A.G., Smith L.M.II. 2002. Biology and management of the smokybrown cockroach. Annual Reviews of Entomology, 47, 33–55. DOI: 10.1146/annurev.ento.47.091201.145106

    Article  CAS  Google Scholar 

  • Barus V., Koubková B. 2002. The first species of Thelastoma Leidy, 1849 (Nematoda: Thelastomatidae) parasitising the scorpion Euscorpius italicus (Chactidae: Scorpionidea). Systematic Parasitology, 53, 141–146

    Article  Google Scholar 

  • Bell W.J. (Ed.) 1981. The Laboratory Cockroach — Experiments in Cockroach Anatomy, Physiology and Behavior. Chapman & Hall, London, UK, pp.161

    Google Scholar 

  • Bell W.J., Adiyodi K.G. 1981. The American Cockroach. Chapman and Hall, London, pp.529

    Book  Google Scholar 

  • Bell W.J., Roth L.M., Nalepa C.A. (Eds.) 2007. Cockroaches: ecology, behavior, and natural history. The Johns Hopkins University Press, Baltimore, Maryland, USA, pp.230

    Google Scholar 

  • Biswas P.K., Chakravarty G.K 1963. The systematic studies of the zoo-parasitic oxyuroid nematodes. Zeitschrift für Parasitenkunde, 23, 411–428

    Article  CAS  Google Scholar 

  • Blanco M.V., Lax P., Dueñas J.C.R., Gardenal C.N., Doucet M.E. 2012. Morphological and molecular characterization of the entomoparasitic nematode Hammerschmidtiella diesingi (Nematoda, Oxyurida, Thelastomatidae). Acta Parasitologica, 57, 302–310. DOI: 10.2478/s11686-012-0029-2

    Article  Google Scholar 

  • Camino N.B., Ricuzzi M., Costa L.L. 2013. A new Thelastomatidae, Hammerschmidtiella laplate n. sp. (Nematoda) parasite of the cockroach Periplaneta americana (L.) (Blattodea, Blattidae) from Argentina. Neotropical Helminthology, 7, 96–103

    Google Scholar 

  • Chaudhary A., Kansal G., Singh N., Singh H. S. 2014. New molecular data for parasite Hammerschmidtiella indicus and Thelandros scleratus (Nematoda; Oxyurida) to infer phylogenetic position. Turkish Journal of Zoology, 38, 1–5. DOI: 10.3906/zoo-1311-18

    Article  Google Scholar 

  • Christie J.R. 1931. Some nemic parasites (Oxyuridae) of coleopterous larvae. Journal of Agricultural Research, 42, 463–482

    Google Scholar 

  • Chilton N.B., Gasser R.B., Beveridge I. 1995. Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). International Journal for Parasitology, 25, 647–651

    Article  CAS  Google Scholar 

  • Chitwood B.G. 1932. A synopsis of the nematodes parasitic in insects of the family Blattidae. Zeitschrift für ParasitenKunde, 5, 14–50

    Article  Google Scholar 

  • Connor S., Adamson M. 1998. Niche overlap among three species of pinworm parasitic in the hindgut of the American cockroach, Periplaneta americana. Journal of Parasitology, 84, 245–247

    Article  CAS  Google Scholar 

  • de Magalhães P.S. 1900. Notes d´Helminthologie Brésilienne. Archives de Parasitologie, 3, 34–69. (In French)

    Google Scholar 

  • Dollfus R.P. 1952. Quelques Oxyuroidea de Myriapodes. Annales de Parasitologie Humaine et Comparée, 27, 143–236. (In French)

    Article  CAS  Google Scholar 

  • Dobrovolny C.G., Ackert J.E. 1934. The life history of Leidynema appendiculatum (Leidy), a nematode parasite of cockroaches. Parasitology, 26, 468–480

    Article  Google Scholar 

  • Felsenstein J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791

    Article  Google Scholar 

  • Groschaft J. 1956. Studies on the Oxyuroidea from cockroaches (Blattodea) in the laboratory. Ceskonslovenska Parasitologie, 3, 67–74 (In Czech)

    Google Scholar 

  • Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98

    CAS  Google Scholar 

  • Hasegawa K., Mota M.M., Futai K., Miwa J. 2006. Chromosome structure and behavior in Bursaphelenchus xylophilus (Nematoda: Parasitaphelenchidae) germ cells and early embryo. Nematology, 8, 425–434. DOI: 10.1163/156854106778493475

    Article  Google Scholar 

  • Hominick W.M., Davey K.G. 1972. The influence of host stage and sex upon the size and composition of the population of two species of thelastomatids parasitic in the hindgut of Periplaneta americana. Canadian Journal of Zoology, 50, 947–954

    Article  Google Scholar 

  • Jex A.R., Hu M., Rose H.A., Schneider T.H., Cribb T.H., Gasser R.B. 2006. Molecular characterization of Thelastomatoidea (Nematoda: Oxyurida) from cockroaches in Australia. Parasitology, 133, 123–129. DOI: https://doi.org/10.1017/S0031182006009978

    Article  CAS  Google Scholar 

  • Kimura M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120. DOI: 10.1007/BF01731581

    Article  CAS  Google Scholar 

  • Khairul A.A., Paran T.P. 1977. Parasites of Periplaneta americana Linn., in Penang, Malaysia I. Thelastoma malaysiense, new species, with notes on Hammerschmidtiella diesingi and Leidynema appendiculata. Malayan Nature Journal, 30, 69–77

    Google Scholar 

  • Koubková B., Barus V., Matejusová I., Hodová I., Koubek P. 2006. Thelastoma gueyei sp. n. (Nematoda: Thelastomatidae) from the Senegal diplopod Archispirostreptus tumuliporus (Diplopoda: Spirostreptidae). Nematology, 8, 739–747

    Article  Google Scholar 

  • McCallister G.L. 1988. The Effect of Thelastoma bulhoesi and Hammerschmidtiella diesingi (Nematoda: Oxyurata) on Host Size and Physiology in Periplaneta americana (Arthropoda: Blattidae). Proceedings of the Helminthological Society of Washington, 55, 12–14

    Google Scholar 

  • McCallister, G.L. 1993. The Effect of Temperature, pH, Sodium Chloride, and Glucose on the Survival of Female Thelastoma bulhoesi (Nematoda: Oxyurata). Proceedings of the Helminthological Society of Washington, 60, 170–173

    Google Scholar 

  • McCallister G.L., Schmidt G.D. 1981. Diurnal Migration of the Female of Thelastoma bulhoesi (Oxyurata: Thelastomida) in the American Cockroach, Periplaneta americana. Proceedings of the Helminthological Society of Washington, 48, 127–129

    Google Scholar 

  • McCallister G. and Schmidt, G.D. 1983. Development of Thelastoma bulhoesi (Oxyurata: Thelastomatida) and the effect of Thiabendazole on the unembryonated egg. Journal of Nematology, 15, 296–301

    PubMed  PubMed Central  CAS  Google Scholar 

  • McCallister G., Schmidt, G.D. 1984. Effect of temperature on the development of Thelastoma bulhoesi (Oxyurata, Thelastomatida) and other nematodes. Journal of Nematology, 16, 355–360

    PubMed  PubMed Central  CAS  Google Scholar 

  • Morffe J., García N. 2010. Hystrignathus dearmasi sp. n. (Oxyurida, Hystrignathidae), first record of a nematode parasitizing a Panamanian Passalidae (Insecta, Coleoptera). Zookeys, 57, 1–8. DOI: /10.3897/zookeys.57.477

    Article  Google Scholar 

  • Nedelchev, S., Pilarska, D., Takov, D., Golemansky, V. 2013. Protozoan and Nematode Parasites of the American Coakroach Periplaneta americana (L.) from Bulgaria. Acta Zoologica Bulgarica, 65, 403–408

    Google Scholar 

  • Nunn G.B. 1992. Nematode molecular evolution. An investigation of evolutionary patterns among nematodes based upon DNA sequences. Ph. D. dissertation. University of Nottingham, UK, pp. 187

    Google Scholar 

  • Osche G. 1960. Systematische, morphologische uns parasitophyletische Studienanparasitischen Oxyuroidea (Nematoda) exotischer Diplopoden (Ein Beitrag zur Morphologie des Sexualdimorphismus). Zoologische Jahrbücher. Abteilung für Systematik, Oecologie und Geographie der Tiere, 87, 395–440. (In German)

    Google Scholar 

  • Ozawa S., Vicente C.S.L., Sato K., Yoshiga T., Kanzaki N., Hasegawa K. 2014. First report of the nematode Leidynema appendiculata from Periplaneta fuliginosa. Acta Parasitologica, 59, 219–228

    Article  Google Scholar 

  • Rentz D. (Ed). 2014. A guide to the cockroaches of Australia. CSIRO Publishing, Australia, pp. 318

    Google Scholar 

  • Ruiz J.M., Coelho E. 1955. Nematóides (Oxyuroidea) parasitos de Diplópodos da Ilha da Queimada Grande, São Paulo, Brasil. Memorias do Instituto Butantan, 27, 51–66. (In Portuguese)

    Google Scholar 

  • Saitou N., Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biological Evolution, 4, 406–425

    CAS  Google Scholar 

  • Shah, M.M. 2007. Some studies on insect parasitic nematodes (Oxyurida, Thelastomatoidea, Thelastomatidae) from Manipur, North-East India. Acta Parasitologica, 52, 346–362

    Google Scholar 

  • Shaham S. 2006. Methods in Cell Biology. In: The C. elegans Research Community (ed.). WormBook, https://doi.org/www.wormbookorg. DOI: doi/10.1895/wormbook.1.49.1

    Google Scholar 

  • Shinya R., Hasegawa K., Chen A., Kanzaki N., Sternberg P. 2014. Evidence of hermaphroditism and sex ratio distortion in the fungal feeding nematode Bursaphelenchus okinawaensis. G3Genes Genomes Genetics, 4, 1907–1917. DOI: 10.1534/g3.114.012385

    Google Scholar 

  • Singh H.S., Kaur H. 1988. On a new nematode, Hammerschmidtiella bisiri n. sp. from Periplaneta americana Linn. Indian Journal of Parasitology, 12, 187–189

    Google Scholar 

  • Spiridonov S.E., Guzeeva E.A. 2009. Phylogeny of nematodes of the superfamily Thelastomatoidea (Oxyurida) inferred from LSU rDNA sequence. Russian Journal of Nematology, 17, 127–134.

    Google Scholar 

  • Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biological Evolution, 28, 2731–2739. DOI: 10.1093/molbev/msr121

    Article  CAS  Google Scholar 

  • The Japanese Society of Pestology. 2014 Pest distribution record 2014. Pestology, 29, 62. (In Japanese)

    Google Scholar 

  • Todd A.C. 1944. On the development and hatching of the eggs of Hammerschmidtiella diesingi and Leidynema appendiculatum, nematodes of roaches. Transactions of the American Microscopical Society, 63, 54–67

    Article  Google Scholar 

  • Van Waerebeke D. 1987. Description de Thelastoma gipetiti n. sp. parasite de Spirostreptidae et considérations sur le genre Thelastoma Leidy, 1850 (Oxyuroidea; Nematoda). Revue Nématologie, 10, 401–407

    Google Scholar 

  • Yoshida K., Hasegawa K., Mochiji N., Miwa J. 2009. Early embryogenesis and anterior-posterior axis formation in the whiteip nematode Aphelenchoides besseyi. Journal of Nematology, 41, 17–22

    PubMed  PubMed Central  Google Scholar 

  • Zervos S. 1983. Blatticola monandros n. sp. (Nematoda: Thelastomatidae) from the blattellid cockroach Parellipsidon pachycercum. New Zealand Journal of Zoology 10, 329–334

    Article  Google Scholar 

  • Zervos S. 1988. Evidence for population self-regulation, reproductive competition and arrhenotoky in a thelastomatid nematode of cockroaches. Parasitology, 96, 369–379. DOI: https://doi.org/10.1017/S0031182000058352

    Article  Google Scholar 

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Correspondence to Koichi Hasegawa.

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Sota Ozawa and Jans Morffe contributed equally to this work and should be consider as first co-authors Author’s

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Ozawa, S., Morffe, J., Vicente, C.S.L. et al. Morphological, molecular and developmental characterization of the thelastomatid nematode Thelastoma bulhoesi (de Magalhães, 1900) (Oxyuridomorpha: Thelastomatidae) parasite of Periplaneta americana (Linnaeus, 1758) (Blattodea: Blattidae) in Japan. Acta Parasit. 61, 241–254 (2016). https://doi.org/10.1515/ap-2016-0034

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