Abstract
Forty-four specimens of the millipede Narceus gordanus Chamberlin, 1943 (Spirobolida: Spirobolidae) were collected from Alachua, Citrus, Hernando, and Marion counties in peninsular Florida. Morphometric data were recorded for each. Nematodes were dissected from the intestine of each individual and sorted into morphotaxa. Heth pivari n. sp. (Oxyuridomorpha: Ransomnematoidea: Hethidae) was found in 33 (75%) of dissected N. gordanus and examined with brightfield, differential interference contrast, phase contrast and scanning electron microscopies. LSU rDNA sequences of representative males and females of H. pivari n. sp. were analyzed and compared to sequences of nematodes in the infraorder Rhigonematomorpha. Heth mauriesi, an introduced species, also was sequenced. Females of H. pivari n. sp. differ from those of other Heth spp. in having smooth, button-like somatic and cervical papillae and shallow, shield-like cervical collars. Males have slit-like or narrowed, rather than circular, stomal openings. Heth pivari n. sp. is the first species of this genus found in an indigenous millipede north of Mexico. Keys based on female cervical ornamentation are provided to differentiate the 52 known Heth spp.
References
Adamson, M.L. (1982) Two new species of Heth Cobb, 1898 (Nematoda, Rhigonematidae), from South American diplopods. Bulletin de Muséum National de Histoire Naturelle 4e Série Section, A4, 405–418.
Adamson, M.L. (1983) Redescriptions of five species of Heth Cobb, 1898 (Rhigonematidae: Nematoda) from South American diplopods. Systematic Parasitology, 5, 185–202.
https://doi.org/10.1007/BF00009351
Adamson, M.L. (1985) Rhigonematida (Nematoda) of Rhinocricus bernardinensis (Rhinocricidae, Spirobolida: Diplopoda) with comments on r– and K–selection in nematode parasites of diplopods. Revue Suisse de Zoologie, 92, 871–896.
https://doi.org/10.5962/bhl.part.81920
Adamson, M.L. (1987) Nematode parasites of Orthoporus americanus (Diplopoda: Spirobolida) from Paraguay. Canadian Journal of Zoology, 65 (12), 3011–3019.
https://doi.org/10.1139/z87-456
Artigas, P. (1929) Systematica dos nematoideos dos arthropods. Ph.D. dissertation, Faculdade de Medicina de São Paulo, 113 pp.
Blaxter, M. & Koutsovoulos, G. (2015) The evolution of parasitism in Nematoda. Parasitology, 142 (Supplement 1), S26–S39.
https://doi.org/10.1017/S0031182014000791
Bowie, J.Y. (1985) New species of rhigonematid and thelastomatid nematodes from indigenous New Zealand millipedes. New Zealand Journal of Zoology, 12, 485–503.
https://doi.org/10.1080/03014223.1985.10428300
Bumbarger, D.J., Crum, J., Ellisman, M.H. & Baldwin, J.G. (2006) Three-dimensional reconstruction of the nose epidermal cells in the microbial feeding nematode, Acrobeles complexus (Nematoda: Rhabditida). Journal of Morphology, 267, 1257–1272.
https://doi.org/10.1002/jmor.10456
Carreno, R.A., Ordosch, D., Koltek, J.K., Hamil, D.R. & Tuhela, L. (2013) First United States records of the rhigonematid genera Heth and Ruizia (Nematoda: Rhigonematida) from the introduced millipede, Anadenobolus monilicornis (Diplopoda: Rhinocricidae) in Key Largo, Florida, U.S.A. Comparative Parasitology, 80 (2), 225–232.
https://doi.org/10.1654/4614.1
Caveness, F.E. (1964) A Glossary of nematological terms. Pacific Printers, Ibadan, 83 pp.
Chitwood, B.G. & Chitwood, M.B. (1950) An introduction to nematology. Monumental Printing, Baltimore, Maryland, 213 pp.
Chitwood, M.B. (1935) Two new nematodes from the genus Heth Cobb, 1989 (Atracidae). Proceedings of the Helminthological Society of Washington, 2 (1), 50–51.
Cloudsley-Thompson, J.L. (1949) The significance of migration in myriapods. The Annals and Magazine of Natural History, Series 12, 2 (24), 947–962.
https://doi.org/10.1080/00222934908654037
Cobb, N.A. (1898) Extract from MS report on the parasites of stock. Agricultural Gazette of New South Wales, 9, 296–321 + 419–454.
Crawford, C.S., Minion, G.P. & Boyers, M.D. (1983) Intima morphology, bacterial morphotypes, and effects of annual molt on microflora in the midgut of the desert millipede, Orthoporus ornatus (Girard) (Diplopoda: Spirostreptidae). International Journal of Insect Morphology and Embryology, 12 (5/6), 301–312.
https://doi.org/10.1016/0020-7322(83)90025-9
Crites, J.L. (1964) A millipede, Narceus americanus, as a natural intermediate host of an acanthocephalan. Journal of Parasitology, 50 (2), 293.
https://doi.org/10.2307/3276289
De Ley, P. & Blaxter, M.L. (2002) Systematic position and phylogeny. In: Lee, D.L. (Ed.), The biology of nematodes. Taylor & Francis, London, pp. 1–30.
https://doi.org/10.1201/b12614-2
Dollfus, R. Ph. (1952) Quelques Oxyuroidea de myriapodes. Annales de Parasitologie Humaine et Comparee, 27, 146–236.
https://doi.org/10.1051/parasite/1952271143
García, N. & Coy, A. (1995) Nuevas especies de nemátodos (Nematoda) de arthópodos Cubanos. Avicennia, 3, 87–96.
García, N. (1997) Nuevas especies de nematodos (Nematoda: Rhigonematida) parasitos de Rhinocricus suprenans (Diplopoda: Spirobolida) en Cuba. Avicennia, 6/7, 6–14.
García, N., Coy, A. & Ventosa, L. (2001) Tres especies nuevas de rigonemátidos (Nematoda: Rhigonematida), parásitos de diplópodos (Diplopoda: Spirobolida) de La Española. Solenodon, 1, 25–32.
García, N. & Fontenla, J.L. (2004) Especies nuevas de nemátodes (Nematoda: Rhigonematida) asociados con Anadenobolus a. arboreus (Diplopoda: Rhinocricidae) de Puerto Rico. Solenodon, 4, 6–10.
Hash J.M. & Brown, B.V. (2015) Revision of the New World species of the millipede-parasitic genus Myriophora Brown (Diptera: Phoridae). Zootaxa, 4035 (1), 1–79.
https://doi.org/10.11646/zootaxa.4035.1.1
Hunt, D.J. (1994) A synopsis of the Hethidae (Nematoda: Rhigonematida) with descriptions of five new species of Heth Cobb, 1898 from diplopods from Papua New Guinea. Russian Journal of Nematology, 2, 15–31.
Hunt, D.J. (1996) Travassosinema thyropygi sp. n. (Nematoda: Travassosinematidae) from a spirobolid millipede from Vietnam with SEM observations on Heth imias Spiridonov, 1989 (Nematoda: Hethidae). Fundamental and Applied Nematology, 19 (1), 7–14.
Kloss, G.R. (1961) Parasitos intestinalis do Diplopoda Scaphiostreptus buffalus Schuart. Boletim Do Museu Paraense Emilo Goeldi. Nova série. Anthropologia, 35, 1–13.
Kloss, G.R. (1965) Compêndio dos nematóides parasitos intestinais de artrópodos. III. Carnoyidae e Hethidae. Arquivos de Zoologia, 13, 47–137.
Leidy, J. (1853) A flora and fauna within living animals. Smithsonian Contributions to Knowledge, 5, 46–48.
https://doi.org/10.5962/bhl.title.56319
Maddison, W.P. & Maddison, D.R. (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75. [http://mesquiteproject.org]
Malysheva, S.V. & Cribb, T.H. (2012) A new species of Heth Cobb, 1898 (Nematoda: Rhigonematida: Hethidae) from an Australian millipede (Myriapoda: Diplopoda: Spirostreptida). New Zealand Journal of Zoology, 39 (4), 301–309.
https://doi.org/10.1080/03014223.2012.672435
Malysheva, S.V., Mohagan, A.B. & Spiridonov, S.E. (2015) Heth impalutiensis n. sp. (Nematoda: Ransomnematoidea: Hethidae) a millipede parasite from Central Mindanao, Philippines. Zootaxa, 3926 (1), 110–110.
https://doi.org/10.11646/zootaxa.3926.1.4
Malysheva, S.V. & Spiridonov, S.E. (2010) Four new species of Heth Cobb, 1898 (Rhigonematida: Hethidae) from Vietnamese diplopods. Nematology, 12, 567–585.
https://doi.org/10.1163/138855409X126018972397911
Malysheva, S.V. & Sumaya, N.H.N. (2017) Two new species of Heth Cobb, 1898 (Nematoda: Ransomnematoidea) from Northern Mindanao, the Philippines. Nematology, 19, 1003–1015.
https://doi.org/10.1163/15685411-00003102
Martini, E. (1926) Zur Anatomie des Vorderendes von Oxyuris robusta. Archiv für Schiffs- und Tropen-hygiene, 30, 1–9. [not seen; cited in Chitwood & Chitwood 1950]
Mejía-Madrid, H.H. (2014) Three new species of Heth Cobb, 1898 (Ransomnematoidea: Hethidae) from spirobolid millipedes from Mexico. Nematology, 16, 83–98.
https://doi.org/10.1163/15685411-00002747
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, Louisiana, 14 November 2010, pp. 1–8.
https://doi.org/10.1109/GCE.2010.5676129
Nadler, S.A., Bolotin, E. & Stock, S.P. (2006) Phylogenetic relationships of Steinernema Travassos, 1927 (Nematoda: Cephalobina: Steinernematidae) based on nuclear, mitochondrial and morphological data. Systematic Parasitology, 63, 161–181.
https://doi.org/10.1007/s11230-005-9009-3
Phillips, G., Bernard, E.C. & Shelley, R.M. (2015) Kleptoparasitic nematodes of diplopods in North America and potential pathogenic effects. Journal of Nematology, 47 (3), 262–263.
Phillips, G., Bernard, E.C., Pivar, R.J., Moulton, J.K. & Shelley, R.M. (2016) Coronostoma claireae n. sp. (Nematoda: Rhabditida: Oxyuridomorpha: Coronostomatidae) from the indigenous milliped Narceus gordanus (Chamberlain, 1943) (Diplopoda: Spirobolida) in Ocala National Forest, Florida. Journal of Nematology, 48 (3), 159–169.
https://doi.org/10.21307/jofnem-2017-023
Remy, P.A. (1950) On the enemies of myriapods. The Naturalist, London, 1950, 103–108.
Sánchez-Velázquez, L. (1979) Seis nuevas especies de nemátodos parásitos de diplopodos de México. Anales del Instituto de Biologia, Universidad Nacional Autonoma de Mexico, Serie Zoologica, 50, 63–117.
Schmidt-Rhaesa, A., Farfan, M.A. & Bernard, E.C. (2009) First record of millipeds as hosts for Horsehair worms (Nematomorpha) in North America. Northeastern Naturalist, 16 (1), 125–130.
https://doi.org/10.1656/045.016.0110
Seinhorst, J.W. (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica, 4, 67–69.
https://doi.org/10.1163/187529259X00381
Shelley, R.M. & Bauer, S.B. (1997) Distribution of the milliped Tylobolus utahensis Chamberlin, with remarks on T. fredericksoni (Causey) (Spirobolida: Spirobolidae). Great Basin Naturalist, 57 (3), 231–237.
Shelley, R.M. & Floyd, S.D. (2014) Expanded concept of the milliped family Spirobolidae (Diplopoda: Spirobolida: Spirobolidae): Proposals of Aztecolini n. tribe and Floridobolinae/ini and Tylobolini n. status.; (re)descriptions of Floridobolus and F. penneri, both Causey, 1957, and F. orini n. sp.; hypotheses on origins and affinities. Insecta Mundi, 0357, 1–50.
Shelley, R.M., McAllister, C.T. & Medrano, M.F. (2006) Distribution of the milliped genus Narceus Rafinesque, 1820 (Spirobolida: Spirobolidae); occurrences in New England and west of the Mississippi River; a summary of peripheral localities; and first records from Connecticut, Delaware, Maine, and Minnesota. Western North American Naturalist, 66 (3), 374–389.
https://doi.org/10.3398/1527-0904(2006)66[374:DOTMGN]2.0.CO;2
Spiridonov, S.E. (1989) New species of Rhigonematida (Nematoda) from the Cuban spirobolid Rhinocricus sp. (Diplopoda). Folia Parasitologica, 36, 71–82.
Spiridonov, S.E. & Yushin, V.V. (2000) Ultrastructure of the stoma in Heth mauriesi Adamson, 1982 (Rhigonematida: Hethidae). Nematology, 2, 417–424.
https://doi.org/10.1163/156854100509277
Swofford, D.L. (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
Tantalean, M.V. & Altmann, L.A. (1989) Cinco nematodes parásitos de “milpies” (Diplopoda, Spirostreptidae) de Amazonas-Perú. Revista Peruana de Entomologica, 31, 147–150.
van Waerebeke, D., Noury-Sraĭri, N. & Justine, J.L. (1990) Spermatozoa of rhigonematid nematodes: morphology of 25 species and ultrastructure of Rhigonema madecassum. International Journal for Parasitology, 20 (6), 779–784.
https://doi.org/10.1016/0020-7519(90)90011-B
Wheeler, T.J. & Kececioglu, J.D. (2007) Multiple alignment by aligning alignments. Bioinformatics, 23, 559–568.
https://doi.org/10.1093/bioinformatics/btm226
Wright, K.A. & Thomson, J.N. (1981) The buccal capsule of Caenorhabditis elegans (Nematoda: Rhabditoidea): an ultrastructural study. Canadian Journal of Zoology, 59, 1952–1961.
https://doi.org/10.1139/z81-266
Yushin, V.V. & Spiridonov, S.E. (2000) Ultrastructure of the stoma in Heth mauriesi Adamson, 1982 (Rhigonematida: Hethidae). Nematology, 2 (4), 417–424.