Abstract
The present study contributes to the knowledge of the cestode fauna of species of Styracura de Carvalho, Loboda & da Silva, which is the putative sister taxon of freshwater potamotrygonids—a unique group of batoids restricted to Neotropical freshwater systems. We document species of Rhinebothrium Linton, 1890 as a result of the examination of newly collected specimens of Styracura from five different localities representing the eastern Pacific Ocean and the Caribbean Sea. Overall, we examined 33 spiral intestines, 11 from the eastern Pacific species Styracura pacifica (Beebe & Tee-Van) and 22 from the Caribbean species S. schmardae (Werner). However, only samples from the Caribbean were infected with members of Rhinebothrium. Rhinebothrium tetralobatum Brooks, 1977, originally described from S. schmardae—as Himantura schmardae (Werner)—off the Caribbean coast of Colombia based on six specimens is redescribed. This redescription provides the first data on the microthriches pattern, more details of internal anatomy (i.e., inclusion of histological sections) and expands the ranges for the counts and measurements of several features. We describe a new species of Rhinebothrium from S. schmardae collected off the Caribbean coast of Panama. Rhinebothrium reydai n. sp. is diagnosed by possessing four testes per proglottid, acraspedote proglottids, single anterior-most and porterior-most loculi, and bothridia divided into 34–44 loculi. Collectively, these features distinguish the new species from all 41 species of Rhinebothrium currently recognized as valid, with the exception of R. chollaensis Friggens & Duszynski, 2005. The latter species, a parasite of Urobatis halleri (Cooper) from the eastern Pacific Ocean, has a similar morphology in comparison to R. reydai n. sp., but can be distinguished by being apolytic instead of euapolytic and by the morphology of the aporal lobe of the ovary, which reaches the mid-lateral margin of the cirrus sac, whereas in R. reydai n. sp. the aporal lobe only reaches the posterior margin, since the cirrus sac takes approximately ¾ of the proglottid in width. Also, in R. reydai n. sp., the first square proglottid occurs within the anterior third of the strobila (13–30%), whereas in R. chollaensis it occurs near the middle of the strobila (42–62%). Further, we discuss the patterns of infection and biogeographical distribution for species of Rhinebothrium in species of Styracura. The apparent disjunctive distribution of R. tetralobatum and R. reydai n. sp. in the Caribbean Sea throughout their host distribution, S. schmardae, and the absence of species of Rhinebothrium in the eastern Pacific sister-host, S. pacifica, reveal the importance of sample size and biogeographical representation for documenting the parasite fauna of host lineages.
References
Appy, R. & Dailey, M.D. (1977) A new species of Rhinebothrium (Cestoda: Tetraphyllidea) and redescription of three rhinebothriate species from the round stingray, Urolophus halleri Cooper in southern California. Bulletin of the Southern California Academy of Sciences, 76, 116–127.
Aschliman, N.C. (2011) The Batoid tree of life: Recovering the patterns and timing of the evolution of skates, rays and allies (Chondrichthyes: Batoidea). The Florida State University, Tallahassee, Florida, 184 pp.
Ball, D., Neifar, L. & Euzet, L. (2003) Proposition de Scalithrium n. gen. (Cestoda, Tetraphyllidea) avec comme espèce-type Scalithrium minimum (Van Beneden, 1850) n. comb. parasite de Dasyatis pastinaca (Elasmobranchii, Dasyatidae). Parasite, 10, 31–37.
https://doi.org/10.1051/parasite/2003101p31Blair, D. (1994) So many parasites and so little time! Systematic Biology, 43, 296–298.
https://doi.org/10.2307/2413473
Brooks, D.H. (1977) Six new species of tetraphyllidean cestodes, including a new genus, from a marine stingray Himantura schmardae (Werner, 1904) from Colombia. Proceedings of the Helminthological Society of Washington, 44 (1), 51–59.
Brooks, D.R., Thorson, T.B. & Mayes, M.A. (1981) Fresh-water stingrays (Potamotrygonidae) and their helminth parasites: testing hypotheses of evolution and coevolution. In: Funk, V.A. & Brooks, D.R. (Eds.), Advances in Cladistics, The New York Botanical Gardens, New York, pp. 147–243.
Caira, J.N. (1990) Metazoan parasites as indicators of elasmobranch biology. In: Pratt, H.L., Gruber, S.H. Jr. & Taniuchi, T. (Eds.), Elasmobranchs as living resources: Advances in the biology, ecology, systematics, and the status of the fisheries, NOAA Technical Report 90, NOAA/National Marine Fisheries Service, Silver Springs, pp. 71–96.
Caira, J.N. (1994) Parascript: Paragon or parody. Review of Parascript: Parasites and the language of evolution, by D.R. Brooks & D.A. Mclennan. Bioscience, 44, 771–773.
https://doi.org/10.2307/1312587Caira, J.N., Jensen, K. & Healy, C.J. (1999) On the phylogenetic relationships among tetraphyllidean, lecanicephalidean and diphyllidean tapeworm genera. Systematic Parasitology, 42, 77–151.
https://doi.org/10.1023/A:1006192603349Caira, J.N. & Jensen, K. (2001) An investigation of the coevolutionary relationships between onchobothriid tapeworms and their elasmobranch hosts. International Journal of Parasitology, 31, 960–975.
https://doi.org/10.1016/S0020-7519(01)00206-5Caira, J.N. & Euzet, L. (2001) Age of association between the nurse shark, Ginglymostoma cirratum, and tapeworms of the genus Pedibothrium (Tetraphyllidea: Onchobothriidae): implications from geography. Biological Journal of the Linnean Society, 72, 609–614.
https://doi.org/10.1111/j.1095-8312.2001.tb01341.x
Campbell, R.A. (1970) Notes on tetraphyllidean cestodes from the Atlantic Coast of North America, with descriptions of two new species. Journal of Parasitology, 56, 498–508.
https://doi.org/10.2307/3277613Chervy, L. (2009) Unifed terminology for cestode microtriches: a proposal from the International Workshops on Cestode Systematics in 2002–2008. Folia Parasitologica, 56 (3), 199–230.
https://doi.org/10.14411/fp.2009.025Clopton, R.E. (2004) Standard nomenclature and metrics of plane shapes for use in gregarine taxonomy. Comparative Parasitology, 71, 130–140.
https://doi.org/10.1654/4151Dailey, M.D. & Carvajal, J. (1976) Helminth parasites of Rhinobatos planiceps Garman 1880, including two new species of cestodes, with comments on host specificity of the genus Rhinebothrium Linton, 1890. Journal of Parasitology, 62 (6), 939–942.
https://doi.org/10.2307/3279187de Carvalho, M.R., Loboda. T.S. & Silva, J.P. (2016) A new subfamily, Styracurinae, and new genus, Styracura, for Himantura schmardae (Werner, 1904) and Himantura pacifica (Beebe & Tee-Van, 1941) (Chondrichthyes: Myliobatiformes). Zootaxa, 4175 (3), 201-–221.
http://doi.org/10.11646/zootaxa.4175.3.1de Carvalho, M.R., Maisey, J.G. & Grande, L. (2004) Freshwater stingrays of the Green River formation of Wyoming (early Eocene), with the description of a new genus and species and an analysis of its phylogenetic relationships (Chondrichthyes: Myliobatiformes). Bulletin of the American Museum of Natural History, 284, 1–136.
https://doi.org/10.1206/0003-0090(2004)284%3C0001:FSOTGR%3E2.0.CO;2Dove, A.D.M. & Cribb, T.H. (2006) Species accumulation curves and their application in parasite ecology. Trends in Parasitology, 22 (12), 569–574.
https://doi.org/10.1016/j.pt.2006.09.008Euzet, L. (1953) Cestodes tétraphyllides nouveaux ou peu connus de Dasyatis pastinaca (L.). Annales de Parasitologie Humaine et Comparée, 28, 339–351.
Friggens, M.M. & Duszynski, D.W. (2005) Four new cestode species from the spiral intestine of the round stingray, Urobatis halleri, in the northern Gulf of California, Mexico. Comparative Parasitology, 72 (2), 136–149.
https://doi.org/10.1654/4121Golestaninasab, M. & Malek, M. (2016) Two new species of Rhinebothrium (Cestoda: Rhinebothriidea) from granulated guitarfish Glaucostegus granulatus in the Gulf of Oman. Journal of Helminthology, 90 (4), 441–454.
https://doi.org/10.1017/S0022149X15000553Goteli, N.J. & Colwell, R.K. (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology letters, 4, 379–391.
https://doi.org/10.1046/j.1461-0248.2001.00230.xHealy, C.J., Caira, J.N., Jensen, K., Webster, B.L. & Littlewood, D.T.J. (2009) Proposal for a new tapeworm order, Rhinebothriidea. International Journal of Parasitology, 39 (4), 497–511.
https://doi.org/10.1016/j.ijpara.2008.09.002Huber, P.M. & Schmidt, G.D. (1985) Rhinebothrium biorchidum n. sp., a tetraphyllidean cestode from a yellow-spotted stingray, Urolophus jamaicensis, in Jamaica. Journal of Parasitology, 71 (1), 1–3.
https://doi.org/10.2307/3281968Jensen, K. (2005) Tapeworms of Elasmobranchs (Part I). A monograph on the Lecanicephalidea (Platyhelminthes, Cestoda). Bulletin of the University of Nebraska State Museum, 18, 1–241.
Jordan, D.S. (1908) The law of geminate species. American Naturalist, 42, 73–80.
https://doi.org/10.1086/278905Kamiya, T., O’Dwyer, K., Nakagawa, S. & Poulin, R. (2014) Host diversity drives parasite diversity: Meta-analytical insights into patterns and causal mechanisms. Ecography, 37, 689–697.
https://doi.org/10.1111/j.1600-0587.2013.00571.xLessios, H.A. (2008) The great American schism: Divergence of marine organisms after the rise of the Central American Isthmus. Annual Review of Ecology, Evolution and Systematics, 39, 63–91.
https://doi.org/10.1146/annurev.ecolsys.38.091206.095815Linton, E. (1890) Notes on Entozoa of marine fishes of New England, with descriptions of several new species. Part II. Report of the United States Commissioner of Fisheries (1887), 15, 718–899.
https://doi.org/10.5962/bhl.title.995Lovejoy, N.R. (1997) Stingrays, parasites and Neotropical biogeography: a closer look at Brooks et al.’s hypotheses concerning the origins of Neotropical freshwater rays (Potamotrygonidae). Systematic Biology, 46, 219–230.
https://doi.org/10.1093/sysbio/46.1.218Lovejoy, N.R., Bermingham, E. & Martin, A.P. (1998) South American rays came in with the sea. Nature, 396, 421–422.
https://doi.org/10.1038/24757Marques, F.P.L., Brooks, D.R. & Ureña, H.M. (1996) Two new species of tetraphyllidean cestodes in Himantura pacifica (Chondrichthyies: Myliobatiformes: Dasyatidae). Journal of Parasitology, 82, 302–306.
https://doi.org/10.2307/3284165Marques, F.P.L. (2000) Evolution of Neotropical freshwater stingrays and their parasites: Taking into account space and time. University of Toronto, Ontário, 325 pp.
Marques, F.P.L., Brooks, D.R. & Lasso, C.A. (2001) Anindobothrium n. gen. (Eucestoda: Tetraphyllidea) inhabiting marine and freshwater potamotrygonid stingrays. Journal of Parasitology, 87, 666–672.
https://doi.org/10.1645/0022-3395(2001)087[0666:ANGETI]2.0.CO;2Marques, F.P.L. & Reyda, F.B. (2015) Rhinebothrium jaimei sp. n. (Eucestoda: Rhinebothriidea: Rhinebothriidae): a new species from Neotropical freshwater stingrays (Potamotrygonidae). Folia Parasitologica, 62, 057.
https://doi.org/10.14411/fp.2015.057Marques, F.P.L. & Caira, J.N. (2016) Pararhinebothroides–neither the sister taxon of Rhinebothroides nor a valid genus. Journal of Parasitology, 102 (2), 249–259.
https://doi.org/10.1645/15-894Mojica, K.R., Jensen, K. & Caira, J.N. (2014) The ocellated eagle ray, Aetobatus ocellatus (Myliobatiformes: Myliobatidae), from Borneo and northern Australia as host of four new species of Hornellobothrium (Cestoda: Lecanicephalidea). Journal of Parasitology, 100 (4), 504–515.
https://doi.org/10.1645/13-411.1Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., Straube, N. & Lakner, C. (2012) Elasmobranch Phylogeny: A Mitochondrial Estimate Based on 595 Species. In: Carrier, J.C., Musick, J.A. & Heithaus, M.R. (Eds.), Biology of Sharks and Their Relatives. CRC Press, Boca Raton, pp. 31–56.
https://doi.org/10.1201/b11867-4O’Dea, A., Lessios, H.A., Coates, G.A., Eytan, R.I., Restrepo-Moreno, S.A., Cione, A.L., Collins, L.S., de Queiroz, A., Farris, D.W., Norris, R.D., Stallard, R.F., Woodburne, M.O., Aguilera, O., Aubry, M.P., Berggren, W.A., Budd, A.F., Cozzuol, M.A., Coppard, S.E., Duque-Caro, H., Finnegan, S., Gasparini, G.M., Grossman, E.L., Johnson, K.G., Keigwin, L.D., Knowlton, N., Leigh, E.G., Leonard-Pingel, J.S., Marko, P.B., Pyenson, N.D., Rachello-Dolmen, P.G., Soibelzon, E., Soibelzon, L., Todd, J.A., Vermeij, G.J. & Jackson, J.B.C. (2016) Formation of the Isthmus of Panama. Science Advances, 2 (8), 1–11.
https://doi.org/10.1126/sciadv.1600883Page, R.D.M. & Charleston, M.A. (1998) Trees within trees: Phylogeny and historical associations. Tree, 13, 356–359.
https://doi.org/10.1016/s0169-5347(98)01438-4Paterson, A.M. & Banks, J. (2001) Analytical approaches to measuring cospeciation of host and parasites: through a glass darkly. International Journal for Parasitology, 31, 1012–1022.
https://doi.org/10.1016/S0020-7519(01)00199-0Post, R.J. & Millest, A.L. (1991) Sample size in parasitological and vector surveys. Parasitology Today, 7 (6), 141.
https://doi.org/10.1016/0169-4758(91)90279-wPoulin, R. (2014) Parasite biodiversity revisited: frontiers and constraints. International Journal for Parasitology, 44 (9), 581–589
https://doi.org/10.1016/j.ijpara.2014.02.003Reyda, F.B. & Marques, F.P.L. (2011) Diversification and Species boundaries of Rhinebothrium (Cestoda: Rhinebothriidea) in South American Freshwater Stingrays (Batoidea; Potamotrygonidae). PLoS ONE, 6 (8), 1–26.
https://doi.org/10.1371/journal.pone.0022604Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P. & Cardona, A. (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods, 9 (7), 676–682.
https://doi.org/10.1038/nmeth.2019Spalding, M.D., Fox, H.E., Allen, G.R., Davidson, N., Ferdaña, Z.A., Finlayson, M., Halpern, B.S., Jorge, M.A., Lombana, A., Lourie, S.A., Martin, K.D., McManus, E., Molnar, J., Recchia, C.A. & Robertson, J. (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience, 57 (7), 573–583.
https://doi.org/10.1641/B570707Straney, D.O. (1982) Review of “Advances in cladistics: proceedings of the first meeting of the Willi Hennig society,” edited by Funk, V.A & Brooks, D.R. Systematic Zoology, 31, 337–341.
https://doi.org/10.2307/2413241Thorson, T.B., Brooks, D.R. & Mayes, M.A. (1983) The evolution of freshwater adaptation in stingrays. National Geographic—Research Reports, 15, 663–694.
Vellutini, B.C. & Marques, F.P.L. (2014) WormBox. Available from: https://github. com/nelas/WormBox (accessed 8 January 2014)