Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 4088 No. 4: 11 Mar. 2016
Type: Article
Published: 2016-03-11
DOI: 10.11646/zootaxa.4088.4.3
Page range: 515–530
Abstract views: 118
PDF downloaded: 132

Using Gordiid cysts to discover the hidden diversity, potential distribution,
and new species of Gordiids (Phylum Nematomorpha)

Department of Integrative Biology, 501 Life Sciences West, Oklahoma State University, Stillwater, Oklahoma 74078, U.S.A. Curent address: Alexion Pharmaceuticals Inc.75 Sidney St, Cambridge, Massachusetts 02139 U.S.A.
Department of Integrative Biology, 501 Life Sciences West, Oklahoma State University, Stillwater, Oklahoma 74078, U.S.A.
Department of Integrative Biology, 501 Life Sciences West, Oklahoma State University, Stillwater, Oklahoma 74078, U.S.A.
Zoological Museum and Institute, Biocenter Grindel, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany.
Center for Evolutionary and Theoretical Immunology, Department of Biology, 163 Castetter Hall, University of New Mexico, Albuquerque, New Mexico 87131-0001, U.S.A.
Department of Integrative Biology, 501 Life Sciences West, Oklahoma State University, Stillwater, Oklahoma 74078, U.S.A.
Nematomorpha Gordiida hairworm Gordian worm North America scanning electron microscopy differential interference contrast microscopy non-adult life stages ecological niche models Chordodes Gordius Paragordius Neochordodes COI sequences

Abstract

In this study, we sampled aquatic snails for the presence of hairworm cysts from 46 streams in Payne County, Oklahoma. Gordiid cysts were found at 70 % (32/46) of sites examined. Based on cyst morphology, we were able to identify three morphological types of gordiid cysts, including Paragordius, Gordius, and Chordodes/Neochordodes. Using our gordiid cyst presence data in conjunction with environmental variables, we developed an ecological niche model using Maxent to identify areas suitable for snail infections with gordiids. The model successfully predicted all presence localities of gordiid cysts in snails over a geographic area of 1,810 km2. We used this information, along with arthropod host infections and crowdsourcing, citizen scientists sampling for adult free-living worms during peak emergent times in areas predicted suitable by the model, to document Paragordius varius, Chordodes morgani, and a new species of gordiid (Gordius n. sp.). To our knowledge, this is the first ecological niche model attempted on such a narrow geographic scale (county level) that recovered known locations successfully. We provide new scanning electron micrographs and molecular data for these species. Our field data and ecological niche model clearly indicate that gordiid cysts are easy to detect in the environment and together these sampling techniques can be useful in discovering new species of gordiids, even in relatively well sampled areas for these cryptic parasites.

 

References

  1. Bolek, M.G. & Coggins, J.R. (2002) Seasonal occurrence, morphology, and observations on the life history of Gordius difficilis (Nematomorpha: Gordioidea) from southeastern Wisconsin, United States. Journal of Parasitology, 88, 287–294.
    http://dx.doi.org/10.1645/0022-3395(2002)088[0287:SOMAOO]2.0.CO;2

    Bolek, M.G., Schmidt-Rhaesa, A., Hanelt, B. & Richardson, D.J. (2010) Redescription of the African Chordodes albibarbatus Montgomery 1898, and description of Chordodes janovyi n. sp. (Gordiida, Nematomorpha) and its non-adult stages from Cameroon, Africa. Zootaxa, 2631, 36–54.

    Bolek, M.G., Szmygiel, C., Kubat, A., Schmidt-Rhaesa, A. & Hanelt, B. (2013a) Novel techniques for biodiversity studies of gordiids and description of a new species of Chordodes (Gordiida, Nematomorpha) from Kenya, Africa. Zootaxa, 3717 (1), 23–38.
    http://dx.doi.org/10.11646/zootaxa.3717.1.2

    Bolek, M.G., Rogers, E., Szmygiel, C., Shannon, R.P, Doerfert-Schrader, W.E., Schmidt-Rhaesa, A. & Hanelt, B. (2013b) Survival of larval and cyst stages of gordiids (Nematomorpha) after exposure to freezing. Journal of Parasitology, 99, 397–402.
    http://dx.doi.org/10.1645/12-62.1

    Bolek, M.G., Schmidt-Rhaesa, A., De Villalobos, L.C., Hanelt, B. (2015) Phylum Nematomorpha. In: Thorp, J. & Rogers, D.C. (Eds.), Thorp and Covich's Freshwater Invertebrates. Vol. I. Ecology and General Biology. 4th Edition. Academic Press, Boston, pp. 303–326. [ISBN: 9780123850263]

    Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology in its own terms. Margoilis et.al. revisited. Journal of Parasitology, 83, 575–583.
    http://dx.doi.org/10.2307/3284227

    Camerano, L. (1897) Monografia dei Gordei. Memoire delle Reale Accademia delle Science di Torino, Italy, 47, 339–419.

    Carvalho, J.C.M. (1942) Studies on some Gordiacea of North and South America. Journal of Parasitology, 28, 213–222.
    http://dx.doi.org/10.2307/3272775

    Creplin, C.H. (1847) Chordodes parasitus, ein Schmarotzerwurm aus einer Heuschrecke. Notizen aus dem Gebiete der Naturund Heilkunde, 3, 161–166.

    De Geer, C. (1773) Tipula fusca, antennis simplicibus, descripta. Nova acta Regiae Societatis Scientiarum Upsaliensis, 2, 66–77.

    Derycke, S., Vanaverbeke, J., Rigaux, A., Backeljau, T. & Moens, T. (2010) Exploring the use of cytochrome oxidase c Subunit 1 (COI) for DNA barcoding of free-living marine nematodes. PLoS ONE 5, e13716.
    http://dx.doi.org/10.1371/journal.pone.0013716

    Draparnaud, J.P.R. (1805) Histoire Naturelle des Mollusques Terrestres et Fluviatiles de la France. A. Louis Colas, Paris, 8 + 163 pp., 16 pls.

    Ferri, E., Barbuto, M., Bain, O., Galimberti, A., Uni, S., Guerrero, R., Ferte, H., Bandi, C., Martin, C. & Casiraghi, M. (2009) Integrated taxonomy: traditional approach and DNA barcoding for the identification of filarioid worms and related parasites (Nematoda). Frontiers in Zoology, 6, 1.
    http://dx.doi.org/10.1186/1742-9994-6-1

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.

    Hanelt, B. & Janovy, J. Jr. (1999) The life cycle of a horsehair worm, Gordius robustus (Nematomorpha: Gordioidea). Journal of Parasitology, 85, 135–141.
    http://dx.doi.org/10.2307/3285720

    Hanelt, B., & Janovy, J. Jr. (2002) Morphometric analysis of nonadult characters of common species of American gordiids (Nematomorpha: Gordioidea). Journal of Parasitology, 88, 557–562.
    http://dx.doi.org/10.1645/0022-3395(2002)088[0557:MAONCO]2.0.CO;2

    Hanelt, B. & Janovy, J. Jr. (2003) Spanning the gap: identification of natural paratenic hosts of horsehair worms (Nematomorpha: Gordioidea) by experimental determination of paratenic host specificity. Invertebrate Biology, 122, 12–18.
    http://dx.doi.org/10.1111/j.1744-7410.2003.tb00068.x

    Hanelt, B. & Janovy, J. Jr. (2004) Untying a Gordian knot: the domestication and laboratory maintenance of a Gordian worm, Paragordius varius (Nematomorpha: Gordiida). Journal of Natural History, 39, 939–950.
    http://dx.doi.org/10.1080/0022293021000058718

    Hanelt, B., Grother, L.E. & Janovy, J. Jr. (2001) Physid snails as sentinels of freshwater nematomorphs. Journal of Parasitology, 87, 1049–1053.
    http://dx.doi.org/10.1645/0022-3395(2001)087[1049:PSASOF]2.0.CO;2

    Hanelt, B., Thomas, F. & Schmidt-Rhaesa, A. (2005) Biology of the Phylum Nematomorpha. Advances in Parasitology, 59, 243–305.
    http://dx.doi:10.1016/S0065-308X(05)59004-3

    Hanelt, B., Bolek, M.G. & Schmidt-Rhaesa, A. (2012) Going solo: Discovery of the first parthenogenetic gordiid (Nematomorpha: Gordiida). PLoS ONE, 7, e34472.

    Hanelt, B., Schmidt-Rhaesa, A. & Bolek, M.G. (2015) Cryptic species of a hairworm parasites revealed by molecular data and crowdsourcing of specimen collections. Molecular Phylogenetics and Evolution, 82, 211–218.
    http://dx.doi.org/10.1016/j.ympev.2014.09.010

    Haverkost, T.R., Gardenr, S.L. & Peterson, A.T. (2010) Predicting the distribution of a parasite using the ecological niche model, GARP. Revista Mexicana de Biodiversidad, 8, 895–902.

    Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
    http://dx.doi.org/10.1007/BF01731581

    Leidy, J. (1851) On the Gordiacea. Proceedings of the Academy of Natural Sciences of Philadelphia, 5, 98–100.

    Linné, C. (1758) Systema Naturae. Vol. 1. 10th Edition. Trustees of the British Museum, Natural History, London, 824 pp. [from Facsimile 1956]

    McAllister, C.T. & Hanelt, B. (2012) New host and geographical distribution record for Chordodes morgani (Nematomorpha: Gordiida), from Oklahoma. Proceeding of the Oklahoma Academy of Sciences, 92, 75–76.

    McAllister, C.T., Bolek, M.G. & Hanelt, B. (2013) Horsehair worm, Paragordius varius (Nematomorpha: Gordiida): New to the fauna of Oklahoma. The Southwestern Naturalist, 58, 249–250.
    http://dx.doi.org/10.1894/0038-4909-58.2.249

    Montgomery, T.H. (1898) The Gordiacea of certain American collections. Bulletin of the Museum of Comparative Zoology at Harvard College, 32, 23–59.

    Palisot de Beauvois, A.M.F.J. (1817) Insectes recueillis en Afrique et en Amérique, dans les royaumes d'Oware et de Benin, a Saint-Domingue et dans les États-Unis pendant les années 1786–1797. Imprimerie de Fain et Compagnie, Parts 9–10, 137–172. [Paris]

    Peterson, A.T. (2003) Predicting the geography of species’ invasions via ecological niche modeling. The Quartlery Review of Biology, 78, 419–433.
    http://dx.doi.org/10.1086/378926

    Peterson, A.T. (2006) Ecological niche modeling and spatial patterns of disease transmission. Emerging Infectious Diseases, 12, 1822–1826.
    http://dx.doi.org/10.3201/eid1212.060373

    Peterson, A.T., Sanchez-Cordero, V., Beard, B. & Ramsey, J.M. (2002) Ecological niche modeling and potential reservoirs for Chagas disease, Mexico. Emerging Infectious Disease, 8, 662–667.
    http://dx.doi.org/10.3201/eid0807.010454

    Peterson, A.T., Papeş, M. & Soberón, J. (2008) Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecological Modeling, 213, 63–72.
    http://dx.doi.org/10.1016/j.ecolmodel.2007.11.008

    Phillips, S.J., Anderson, R.P. & Schapire, R.E. (2006) Maximum entropy modeling of species geographic distributions. Ecological Modeling, 190, 231–259.
    http://dx.doi.org/10.1016/j.ecolmodel.2005.03.026

    Phillips, S.J. & Dudik, M. (2008) Modeling of species distributions with MAXENT: New extensions and a comprehensive evalution. Ecography, 31, 161–175.
    http://dx.doi.org/10.1111/j.0906-7590.2008.5203.x

    Poinar, G.O. & Weissman, D.B. (2004) Hairworm and nematode infections of North American Jerusalem crickets, field crickets, and katydids (Orthoptera; Stenopelmatidae, Gryllidae and Tettigonidae). Journal of Orthopteran Research, 13, 143–147.
    http://dx.doi.org/10.1665/1082-6467(2004)013[0143:HANION]2.0.CO;2

    Poulin, R. (1998) Book Review: Nematomorpha. Journal of Parasitology, 84, 35.
    http://dx.doi.org/10.2307/3284525

    Raxworthy, C.J., Martínez-Meyer, E., Horning N., Nussbaum, R.A., Schneider, G.E., Ortega-Huerta, M.A. & Peterson, A.T. (2003) Predicting distributions of known and unknown reptile species in Madagascar. Nature, 426, 837–841.
    http://dx.doi.org/10.1038/nature02205

    Redlich, A. (1980) Description of Gordius attoni sp. n. (Nematomorpha, Gordiidae) from Northern Canada. Canadian Journal of Zoology, 58, 382–385.
    http://dx.doi.org/10.1139/z80-049

    Ristau, K., Steinfartz, S. & Traunspurger, W. (2013) First evidence of cryptic species diversity and significant population structure in a widespread freshwater nematode morphospecies (Tobrilus gracilis). Molecular Ecology, 22, 4562–4575.
    http://dx.doi.org/10.1111/mec.12414

    Schmidt-Rhaesa, A. (1997) Nematomorpha. In: Schwoerbel, J. & Zwick, P. (Eds.), Süßwasserfauna Mitteleuropas. Gustav Fischer Verlag, Stuttgart, pp. 1–124.

    Schmidt-Rhaesa, A. (2013) Nematomorpha. In: Schmidt-Rhaesa, A. (Ed.), Handbook of Zoology. Gastrotricha, Cycloneuralia and Gnathifera. Nematomorpha, Priapulida, Kinorhyncha and Loricifera. Vol. 1. De Gruyter, Berlin, pp. 29–145.

    Schmidt-Rhaesa, A., Hanelt, B. & Reeves, W.K. (2003) Redescription and compilation of Nearctic freshwater Nematomorpha (Gordiida), with the description of two new species. Proceedings of the Academy of Natural Sciences of Philadelphia, 153, 77–117.
    http://dx.doi.org/10.1635/0097-3157(2003)153[0077:RACONF]2.0.CO;2

    Schmidt-Rhaesa, A., de Villalobos, L.C. & Zanca, F. (2008) Summary of Chordodes species (Nematomorpha, Gordiida), with a discussion of their diagnostic characters. Verhandlungen des Naturwissenschaftlichen Vereins Hamburg, 44, 37–114.

    Schmidt-Rhaesa, A., De Villalobos, C., Zanca, F., Hanelt, B. & Bolek, M.G. (2016) Phylum Nematomorpha. In: Thorp, J. & Rogers, D.C. (Eds.), Thorp and Covich's Freshwater Invertebrates. Vol. II. Keys to Nearctic Fauna. 4th Edition. Academic Press, Boston, pp. 181–188. [ISBN: ISBN-10: 0123850282]
    http://dx.doi.org/10.1016/b978-0-12-385028-7.00010-x

    Sokal, R.R. & Rohlf, J.F. (1981) Biometry. 2nd Edition. W. H. Freeman and Company, New York, New York, 859 pp.

    Szmygiel, C., Schmidt-Rhaesa, A., Hanelt, B. & Bolek, M.G. (2014) Comparative descriptions of non-adult stages of four genera of Gordiids (Phylum: Nematomorpha). Zootaxa, 3768 (2), 101–118.
    http://dx.doi.org/10.11646/zootaxa.3768.2.1

    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 Biology and Evolution, 28, 2731–2739.
    http://dx.doi.org/10.1093/molbev/msr121