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Acta Parasitologica

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Volume 59, Issue 2 (Jun 2014)

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First report of the nematode Leidynema appendiculata from Periplaneta fuliginosa

Sota Ozawa
  • Department of Environmental Biology, College of Bioscience & Biotechnology, Chubu University., 1200 Matsumoto, Kasugai, Aichi, 487-8501, Japan
  • Email:
/ Cláudia Vicente
  • Department of Environmental Biology, College of Bioscience & Biotechnology, Chubu University., 1200 Matsumoto, Kasugai, Aichi, 487-8501, Japan
  • ICAAM — Instituto de Ciências Agrárias e Ambientais Mediterrânicas, Departamento de Biologia, Universidade de Évora, Núcleo da Mitra, Ap. 94, 7002-554, Évora, Portugal
  • Email:
/ Kazuki Sato
  • Laboratory of Terrestrial Microbial Ecology, Graduate School of Agriculture, Kyoto University, Sakyo, Kyoto, 606-8502, Japan
  • Email:
/ Toyoshi Yoshiga
  • Laboratory of Nematology, Department of Applied Biological Sciences, Faculty of Agriculture, Saga University, Saga, 840-8502, Japan
  • Email:
/ Natsumi Kanzaki
  • Forest Pathology Laboratory, Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki, 305-8687, Japan
  • Email:
/ Koichi Hasegawa
  • Department of Environmental Biology, College of Bioscience & Biotechnology, Chubu University., 1200 Matsumoto, Kasugai, Aichi, 487-8501, Japan
  • Email:
Published Online: 2014-05-15 | DOI: https://doi.org/10.2478/s11686-014-0230-6

Abstract

The smokybrown cockroach Periplaneta fuliginosa has spread all over the world, and is now one of the most undesired invasive alien pests in Japan. Because cockroaches are generally infected by thelastomatid nematodes, they are being distributed around the world with their parasitic nematodes. Nothing is known about parasitic nematode species in P. fuliginosa differences, or similarity of the parasite’s population structures between the different countries of the host cockroaches. Here we investigated the P. fuliginosa invasive to Japan and found that 100% of individuals were infected with one nematode species. According to the morphology and the sequence of the D2/D3 expansion segment of the 28S ribosomal RNA gene, we identified the parasite as Leidynema appendiculata. This nematode reproduced by haplodiploidy and its developmental timing under various conditions is quite divergent. Their population in the hindgut of P. fuliginosa was controlled with a few adult females and a male. This is the first report of the thelastomatid nematode isolated from the smokybrown cockroach, and is the basis for our future research examining the origin, distribution route and immigration history of the cockroach and the impact of L. appendiculata on native Japanese cockroach species.

Keywords: Smokybrown cockroach; Periplaneta fuliginosa; invasive alien species; sanitary pest; Japan; Leidynema appendiculata

  • [1] 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. http://dx.doi.org/10.2307/3283057 [Crossref]

  • [2] Adamson M.L., van Waerebeke D. 1992. Revision of the Thelastomatidea, Oxyurida of invertebrate hosts I. Thelastomatidae. Systematic Parasitology, 21, 21–63. http://dx.doi.org/10.1007/BF00009911 [Crossref]

  • [3] 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. http://dx.doi.org/10.2307/3283276 [Crossref]

  • [4] Adamson M.L. 1994. Evolutionary patterns in life histories of Oxyurida. International Journal for Parasitology, 24, 1167–1177. http://dx.doi.org/10.1016/0020-7519(94)90189-9 [Crossref]

  • [5] Ainsworth R. 1991. Cytogenetic evidence of haplodiploidy in two species of nematode (Pharyngodonidae: Oxyurida) from New Zealand lizards. Journal of Parasitology, 77, 92–98. http://dx.doi.org/10.2307/3282564 [Crossref]

  • [6] 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. http://dx.doi.org/10.1146/annurev.ento.47.091201.145106 [Crossref]

  • [7] Asahina S. (Ed.) 1991. Blattaria of Japan. Nakayama Shoten, Tokyo, Japan, 253 pp.

  • [8] Bhatnagar K.N., Edward L.J. 1970. Parasites of the Madagascar cockroach Gromphadorhina portentosa. Annals of the Entomological Society of America, 63, 620–621. [Crossref]

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

  • [10] 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, 230 pp.

  • [11] Blanco M.V., Lax P., Dueñas J.C.R., Gardenal C.N., Doucet M.E. 2012. Morphological and molecular characterization of the entomoparasitic nematode Hammarschmiditiella diesingi (Nematoda, Oxyurida, Thelastomatidae). Acta Parasitologica, 57, 302–310. DOI: 10.2478/s11686-012-0029-2. http://dx.doi.org/10.2478/s11686-012-0029-2 [Web of Science] [Crossref]

  • [12] Chitwood B. 1932. A synopsis of the nematodes parasitic in insects of the family Blattidae. Parasitology Research, 5, 14–50.

  • [13] 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. http://dx.doi.org/10.2307/3284477 [Crossref]

  • [14] Dobrovolny C.G., Ackert J.E. 1934. The life history of Leidynema appendiculata (Leidy), a nematode parasite of cockroaches. Parasitology, 26, 468–480. http://dx.doi.org/10.1017/S0031182000023787 [Crossref]

  • [15] Felsenstein J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39, 783–791. http://dx.doi.org/10.2307/2408678 [Crossref]

  • [16] Galli M. van der Heuvel S. 2008 Determination of the cleavage plane in early C. elegans embryos. Annual Review of Genetics, 42, 389–411. DOI: 10.1146/annurev.genet.40.110405.09 0523 http://dx.doi.org/10.1146/annurev.genet.40.110405.090523 [Crossref] [Web of Science]

  • [17] Grimaldi D., Engel M.S. (Eds.). 2005. Evolution of the insects. Cambridge University Press, Cambridge, UK, 772 pp.

  • [18] 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.

  • [19] Hasegawa K., Futai K., Miwa S., Miwa J. 2004. Early embryogenesis of the pinewood nematode Bursaphelenchus xylophilus. Development Growth and Differentiation, 46, 153–161. DOI: 10.1111/j.1440-169X.2003.00734.x. http://dx.doi.org/10.1111/j.1440-169X.2003.00734.x [Crossref]

  • [20] 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: 10.1163/15685410 6778493475. http://dx.doi.org/10.1163/156854106778493475 [Crossref]

  • [21] 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. http://dx.doi.org/10.1139/z72-127 [Crossref]

  • [22] Hominick W.M., Davey K.G. 1973. Food and the spatial distribution of adult female pinworms parasitic in the hindgut of Periplaneta americana L. International Journal for Parasitology, 3, 759–771. http://dx.doi.org/10.1016/0020-7519(73)90067-2 [Crossref]

  • [23] Jex A.R., Schneider M.A., Rose H.A., Cribb T.H. 2005. The Thelastomatoidea (Nematoda: Oxyurida) of two sympatric Panesthiinae (Insecta: Blattodea) from southeastern Queensland, Australia: taxonomy, species richness and host specificity. Nematology, 7, 543–575. DOI: 10.1163/156854105 774384741. http://dx.doi.org/10.1163/156854105774384741 [Crossref]

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

  • [25] Jex A.R., Schneider T.H., Cribb T.H. 2006b. The importance of host ecology in thelastomatid (Nematoda: Oxyurida) host specificity. Parasitology International, 55, 169–174. DOI: 10.1016/j.parint.2006.03.001. http://dx.doi.org/10.1016/j.parint.2006.03.001 [Crossref]

  • [26] 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. http://dx.doi.org/10.1007/BF01731581 [Crossref]

  • [27] Lee C.Y., Lee L.C. 2000. Influence of sanitary conditions on the field performance of chlorpyrifos-based baits against American cockroaches, Periplaneta americana (L.) (Dictyoptera: Blattdae). Journal of Vector Ecology, 25, 218–221.

  • [28] Miller D.M., Meek F. 2004. Cost and efficacy comparison of integrated pest management strategies with monthly spray insecticide applications for German cockroach (Dictyoptera: Blattellidae) control in public housing. Journal of Economic Entomology, 97, 559–569. http://dx.doi.org/10.1603/0022-0493-97.2.559 [Crossref]

  • [29] Murata K., Hasegawa H., Nakano T., Noda A., Yanai T. 2002. Fatal infection with human pinworm, Enterobius vermicularis, in a captive chimpanzee. Journal of Medical Primatology, 31, 104–108. DOI: 10.1034/j.1600-0684.2002.01017.x. http://dx.doi.org/10.1034/j.1600-0684.2002.01017.x [Crossref]

  • [30] 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.

  • [31] Ogata K., Tanaka I., Ogawa T. 1975. Studies on establishing factors of domiciliary cockroaches. 1. Field surveys of the distribution of domiciliary cockroaches in Tokyo and Kawasaki. Japanese Journal of Sanitary Zoology, 26, 241–245.

  • [32] Poinar G.O. (Ed.). 1975. Entomogenous nematodes: a manual and host list of insect-nematode associations. Brill, Leiden, Netherland, 317 pp.

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

  • [34] Shah M.M. 2007. Some studies on insect parasitic nematodes (Oxyurida, Thelastomatoidea, Thelastomatidae) from Manipur, North-East India. Acta Parasitologica, 52, 346–362. DOI: 10.2478/s11686-007-0051-y. http://dx.doi.org/10.2478/s11686-007-0051-y [Crossref] [Web of Science]

  • [35] Shaham S. 2006. Methods in Cell Biology. In: The C. elegans Research Community (Ed.). WormBook, http://www.wormbook.org. DOI: doi/10.1895/wormbook.1.49.1 [Crossref]

  • [36] Stock S.P. 1988. Leidynema (L.) appendiculata (Nematoda: Thelastomatidae) en larvas de Oncideres sp. (Coleoptera: Cerambycidae) en la Argentina. Revista Peruana de Entomología, 31, 151–153.

  • [37] 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. http://dx.doi.org/10.1093/molbev/msr121 [Crossref] [Web of Science]

  • [38] 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. http://dx.doi.org/10.2307/3223338 [Crossref]

  • [39] Wada-Katsumata A., Silverman J., Schal C. 2013. Changes in taste neurons support the emergence of an adaptive behavior in cockroaches. Science, 340, 972–975. DOI: 10.1126/science. 1234854. http://dx.doi.org/10.1126/science.1234854 [Crossref] [Web of Science]

  • [40] Westphal M.I., Browne A., MacKinnon K., Noble I. 2008. The link between international trade and the global distribution of invasive alien species. Biological Invasion, 10, 391–398. DOI: 10.1007/s10530-007-9138-5. http://dx.doi.org/10.1007/s10530-007-9138-5 [Crossref]

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

  • [42] Zervos S. 1987. Protrellus dalei n. sp., Blatticola barryi n. sp., and Suifunema mackenziei n. sp., thelastomatid nematodes from New Zealand cockroaches. New Zealand Journal of Zoology, 14, 240–250. DOI: 10.1080/03014223.1987. 10422994. [Crossref]

  • [43] Zervos S. 1988a. Population regulation in parasitic nematodes (Thelastomatidae) of cockroaches. New Zealand Journal of Zoology, 15, 333–338. DOI: 10.1080/03014223.1988. 10422622. http://dx.doi.org/10.1080/03014223.1988.10422622 [Crossref]

  • [44] Zervos S. 1988b. Population dynamics of a thelastomatid nematode of cockroaches. Parasitology, 96, 353–368. DOI: http://dx.doi.org/10.1017/S0031182000058340. http://dx.doi.org/10.1017/S0031182000058340 [Crossref]

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

About the article

Published Online: 2014-05-15

Published in Print: 2014-06-01



Citation Information: Acta Parasitologica, ISSN (Online) 1896-1851, DOI: https://doi.org/10.2478/s11686-014-0230-6. Export Citation

© 2014 W. Stefański Institute of Parasitology, PAS. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. (CC BY-NC-ND 3.0)

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