Abstract
We describe a new species of Auriculostoma Scholz, Aguirre-Macedo & Choudhury, 2004 based on several sources of information including morphology (light and scanning electron microscopy [SEM]), sequences of two nuclear genes, host association, and geographical distribution. Morphologically, the new species most closely resembles Auriculostoma astyanace Scholz, Aguirre-Macedo & Choudhury, 2004, but differs by having deeply lobated testes and cirrus-sac extending posteriorly to seminal receptacle level. Auriculostoma lobata n. sp. can be readily distinguished from all the other congeners by the combination of the following characters: testes located in tandem, testes deeply lobated, and larger body size. A phylogenetic analysis using 28S rDNA sequences along with those available for other allocreadiid trematodes, revealed that the new species is a sister taxon of A. astyanace, a species described from the banded astyanax, Astyanax fasciatus (Cuvier) in Nicaragua. Auriculostoma totonacapanensis Razo-Mendivil, Mendoza-Garfias, Pérez-Ponce de León & Rubio-Godoy, 2014 from the Mexican tetra, Astyanax mexicanus (De Filippi) in Mexico is the sister taxon of A. astyanace plus the new species. Genetic divergence levels for the 28S rDNA and ITS2 were estimated among the Middle-American species of Auriculostoma infecting characiforms. The validity of the new species is then established by reliable morphological differences, its host association to bryconids (Brycon guatemalensis Regan), restricted geographical distribution (Usumacinta and Lacantun River basins), and genetic divergence levels, albeit relatively low. A morphometric comparison between the new species and the other seven congeneric species was undertaken and, in addition, a taxonomic key to identify the species contained in the genus Auriculostoma, widely distributed across the Americas, is provided.
References
Abe, K.T., Mariguela, T.C., Avelino, G.S., Foresti, F. & Oliveira, C. (2014) Systematic and historical biogeography of the Bryconidae (Ostariophysi: Characiformes) suggesting a new rearrangement of its genera and an old origin of Mesoamerican ichthyofauna. BMC Evolutionary Biology, 14, 152–152.
http://dx.doi.org/10.1186/1471-2148-14-152Angulo, A. & Gracián-Negrete, J.M. (2013) A new species of Brycon (Characiformes: Characidae) from Nicaragua and Costa Rica, with a key to the lower Mesoamerican species of the genus. Zootaxa, 3731 (2), 255–266.
http://dx.doi.org/10.11646/zootaxa. 3731.2.6Bautista-Hernández, C. E., Monks, S., Pulido-Flores, G. & Miranda, R. (2015) A new species of Paracreptotrema (Digenea, Plagiorchiformes, Allocreadiidae) infecting two species of poeciliids in Río Malila of the Río Pánuco basin, Hidalgo, México, with a key to the species of the genus. ZooKeys, 482, 55–66.
http://dx.doi.org/10.3897/zookeys.482.8144Bowles, J. & McManus, D. P. (1993) Rapid discrimination of Echinococcus species and strains using a PCR-based method. Molecular and Biochemical Parasitology, 57, 231–239.
http://dx.doi.org/10.1016/0166-6851(93)90199-8Bray, R.A., Foster, G.N., Waeschenbach, A. & Littlewood, D.T.J. (2012) The discovery of progenetic Allocreadium neotenicum Peters, 1957 (Digenea: Allocreadiidae) in water beetles (Coleoptera: Dytiscidae) in Great Britain. Zootaxa, 3577, 58–70.
Brooks, D.R. (1992) New distribution records for Bunodera eucaliae and Bunodera inconstans n. comb. (Digenea: Allocreadiidae: Bunoderinae) with discussion of their phylogenetic relationships. Journal of Parasitology, 78, 779–783.
http://dx.doi.org/10.2307/3283303Caspeta-Mandujano, J.M., Moravec, F. & Salgado-Maldonado, G. (2000) Rhabdochona mexicana sp. n. (Nematoda: Rhabdochonidae) from the intestine of characid fishes in Mexico. Folia Parasitologica, 47, 211–215.
http://dx.doi.org/10.14411/fp.2000.039Caspeta-Mandujano, J.M., Cabañas-Carranza, G., Salgado-Maldonado, G., Gosztonyi, A.E. & Cremonte, S. (2005) Nematode parasites of the characid freshwater fish Brycon guatemalensis in the Usumacinta River, Chiapas, Mexico. Helminthologia, 42, 41–44.
Choudhury, A., Daverdin, R.H., & Brooks, D.R. (2002) Wallinia chavarriai n. sp. (Trematoda: Macroderoididae) in Astyanax aeneus (Gunther, 1860) and Bryconamericanus sceloparius (Regan, 1908) (Osteichthyes: Characidae) from the Area de Conservación de Guanacaste, Costa Rica. Journal of Parasitology, 137, 287–302.
Choudhury, A. & León-Règagnon, V. (2005) Molecular phylogenetics and biogeography of Bunodera spp. (Trematoda: Allocreadiidae), parasites of percid and gasterosteid fishes. Canadian Journal of Zoology, 83, 1540–1546.
http://dx.doi.org/10.1139/z05-153Choudhury, A., Pérez-Ponce de León, G., Brooks, D. R. & Daverdin, R. (2006) Paracreptotremata blancoi sp. n. (Digenea: Plagiorchiformes), in the olomina, Priapichthys annectens (Osteichthyes: Poeciliidae) from the Área de Conservación Guanacaste, Costa Rica. Journal of Parasitology, 92, 565–568.
Choudhury, A., Aguirre-Macedo, M.L., Curran, S.S., Ostrowski de Núñez, M., Overstreet, R.M., Pérez-Ponce de León, G. & Portes Santos, C. (2016) Trematode diversity in freshwater fishes of the Globe II: 'New World'. Systematic Parasitology, 93, 271–282.
http://dx.doi.org/10.1645/GE-3540.1Curran, S.S., Pulis, E.E., Hugg, D.O., Brown, J.P., Manuel, L.C., & Overstreet R.M. (2012) Phylogenetic position of Creptotrema funduli in the Allocreadiidae based on partial 28S rDNA Sequences. Journal of Parasitology, 98, 873–875.
http://dx.doi.org/10.1645/GE-3066.1Curran, S.S., Tkach, V.V. & Overstreet, R.M. (2006) A review of Polylekithum Arnold, 1934 and its familial affinities using morphological and molecular data, with description of Polylekithum catahoulensis sp. nov. Acta Parasitologica, 51, 238–248.
http://dx.doi.org/10.2478/s11686-006-0037-1Curran, S.S., Tkach, V.V. & Overstreet, R.M. (2011) Phylogenetic affinities of Auriculostoma (Digenea: Allocreadiidae), with descriptions of two new species from Peru. Journal of Parasitology, 97, 661–670.
http://dx.doi.org/10.1645/GE-2641.1Curran, S.S., Tkach, V. & Overstreet, R.M. (2013) Molecular evidence for two cryptic species of Homalometron (Digenea: Apocreadiidae) in freshwater fishes of the Southeastern United States. Comparative Parasitology, 80, 186–195.
http://dx.doi.org/10.1654/4626.1Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society, 85,407–415.
http://dx.doi.org/10.1111/j.1095–8312.2005.0503.xGarcía-Varela, M. & Nadler, S.A. (2005) Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. Journal of Parasitology, 91, 1401–1409.
Garrido-Olvera, L., García-Prieto, L. & Pérez- Ponce de León, G. (2006) Checklist of the adult nematode parasites of fishes in freshwater localities from Mexico. Zootaxa, 1201, 1–45.
Gendre, E. (1921) Notes d'Helminthologie africaine (sixième note). Procès-Verbaux de la Société Linnéenne de Bordeaux, 73, 148–156.
Hernández-Mena, D.I., García-Prieto, L. & García-Varela, M. (2014) Morphological and molecular differentiation of Parastrigea (Trematoda: Strigeidae) from Mexico, with the description of a new species. Parasitology International, 63, 315–323.
http://dx.doi.org/10.1016/j.parint.2013.11.012Hopkins, S.H. (1931) Studies on Crepidostomum. II. The "Crepidostomum laureatum" of A. R. Cooper. Journal of Parasitology, 18, 79–91.
http://dx.doi.org/10.2307/3271966Jiménez-Guzmán, F. (1973) Tremátodos digeneos de peces dulceacuícolas de Nuevo León, México. I. Dos nuevas especies y un registro nuevo en el caracido Astyanax fasciatus mexicanus (Filippi).Cuadernos del Instituto de Investigaciones Cientificos, Universidad Autónoma de Nuevo León, México, 17, 1–19.
Kasl, E.L., Fayton, T.J., Font, W.F. & Criscione, C.D. (2014) Alloglossidium floridense n. sp. (Digenea: Macroderoididae) from a spring run in North Central Florida. Journal of Parasitology, 100, 121–126.
http://dx.doi.org/10.1645/13–252.1.Kohn, A., Fernandes, B.M. & Cohen, S.C. (2007) South American trematodes parasites of fishes. Ministerio da Saúde, FIOCRUZ, Rio de Janeiro, Brasil, 318 pp.
Lamothe-Argumedo, R. (1970) Tremátodos de peces VI. Margotrema bravoae gen., nov., sp., nov., (Trematoda:Allocreadiidae) parásito de Lermichthys multiradiatus Meek. Anales del Instituto de Biología, Universidad Nacional Autónoma de México, 41, 87–92.
Lima, F.C.T. (2003) Characidae - Bryconinae (Characins, tetras). In: Reis, R.E., Kullander, S.O. & Ferraris, C.J. Jr. (Eds.), Checklist of the Freshwater Fishes of South and Central America. Porto Alegre, EDIPUCRS, Brasil, pp. 174–181.
Looss, A. (1900) Nachträgliche Bemerkungen zu den Namen der von mir vorgeschelagenen Distomengattungen. Zoologischer Anzeiger, 23, 601–608.
Lühe, M. (1909) Parasitische Plattwürmer. I. Trematoden. Die Süsswasserfauna Deutschland, 17, 215–215.
Luton, K., Walker, D. & Blair, D. (1992) Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular & Biochemical Parasitology, 56, 323–327.
http://dx.doi.org/10.1016/0166-6851(92)90181-IMañé-Garzón, F. & Gascón, A. (1973) Digenea de peces de agua dulce de Uruguay, I. Una Nueva especie del genero Crepidostomun Braum, 1900 del intestino de Asiphonichthys stenopterus. Revista de Biología del Uruguay, 1, 11–14.
Miller, R.R., Mickley, W.L. & Norris, S.M. (2005) Freshwater Fishes of Mexico. University of Chicago Press, Chicago, 490 pp.
Mueller, J.F. (1934) Parasites of Oneida Lake fishes. Part IV. Additional notes on parasites of Oneida Lake fishes, including descriptions of new species. Roosevelt Wild Life Annals, 3, 335–373.
Olson, P.D., Cribb, T.H., Tkach, V.V., Bray, R.A. & Littlewood, D.T. (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755.
http://dx.doi.org/10.1016/S0020-7519Pérez-Ponce de León, G., Martínez-Aquino, A. & Mendoza-Garfias, B. (2013) A new species of Margotrema (Digenea, Allocreadiidae) from the Leopard splitfin Xenotaenia resolanae (Cyprinodontiformes, Goodeidae) from west-central Mexico. Zootaxa, 3670 (1), 94–96.
http://dx.doi.org/10.11646/zootaxa.3670.1.10
Pérez-Ponce de León, G., Razo-Mendivil, U., Mendoza-Garfias, B., Rubio-Godoy, M. & Choudhury, A. (2015) A new species of Wallinia Pearse, 1920 (Digenea: Allocreadiidae) in Astyanax mexicanus (Characidae) from Mexico revealed by morphology and sequences of the 28S ribosomal RNA gene. Folia Parasitologica, 62, 18–18.
http://dx.doi.org/10.14411/fp.2015.018Pérez-Ponce de León, G., Pinacho-Pinacho, C.D., Mendoza- Garfias, B., Choudhury, A. & García-Varela, M. (2016) Phylogenetic analysis using the 28S rRNA gene reveals that the genus Paracreptotrema (Digenea: Allocreadiidae) is not monophyletic; description of two new genera and one new species. Journal of Parasitology, 102, 131–142.
Peters, L.E. (1957) An analysis of the trematode genus Allocreadium Looss with the description of Allocreadium neotenicum sp. nov. from water beetles. Journal of Parasitology, 43, 136–142.
http://dx.doi.org/10.1645/15-815Petkevičiūtė, R., Stunzenas, V., Stanevičiūtė, G. & Sokolov, S.G. (2010) Comparison of the developmental stages of some European allocreadiid trematode species and a clarification of their life-cycles based on ITS2 and 28S sequences. Systematic Parasitology, 76, 169–178.
http://dx.doi.org/10.1007/s11230-010-9249-8Pinto, M.R., Noronha, D., Marcelo Knoff, M. & Gomes, D.C. (2010) Rhabdochona (R.) uruyeni (Nematoda, Rhabdochonidae) in Brazil: present status of South American Rhabdochona Railliet with a worldwide bibliographical survey of the genus from 1845 to 2010. Neotropical Helminthology, 4, 49–69.
Platta, C.S. & Choudhury, A. (2006) Systematic position and relationships of Paracreptotrematina limi, based on partial sequences of 28S rRNA and cytochrome c oxidase subunit 1 genes. Journal of Parasitology, 92, 411–413.
http://dx.doi.org/10.1645/GE-3521RN.1Razo-Mendivil, U., Mendoza-Garfias, B., Ponce-Pérez de León, G. & Rubio-Godoy, M. (2014) A new species of Auriculostoma (Digenea: Allocreadiidae) in the Mexican tetra Astyanax mexicanus (Actinopterygii: Characidae) from central Veracruz, Mexico, described with the use of morphological and molecular data. Journal of Parasitology, 100, 331–337.
Salgado-Maldonado, G., Caspeta-Mandujano, J.M., Moravec, F., Soto-Galera, E., Rodiles-Hernández, R., Cabañas-Carranza, G. & Montoya-Mendoza, G. (2011) Helminth parasites of freshwater fish in Chiapas, Mexico. Parasitology Research, 108, 31–59.
http://dx.doi.org/10.1007/s00436-010-2035-3Scholz, T., Aguirre-Macedo, M.L. & Choudhury, A. (2004) Auriculostoma astyanace n. gen., n. sp. (Digenea: Allocreadiidae), from the banded astyanax, Astyanax fasciatus (Characiformes: Characidae), from Nicaragua, with a reevaluation of Neotropical Crepidostomum spp. Journal of Parasitology, 90, 1128–1132.
http://dx.doi.org/10.1645/GE-3275Stafford, J. (1904) Trematodes from Canadian fishes. Zoologischer Anzeiger, 27, 481–495.
Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatic, 22, 2688–90.
http://dx.doi.org/10.1093/bioinformatics/btl446Stamatakis, A., Blagojevic, F., Nikolopoulos, D. & Antonopoulos, C. (2007) Exploring new search algorithms and hardware for phylogenetics: RAxML meets the IBMcell. Journal of VLSI Signal Processing, 48, 271–286.
http://dx.doi.org/10.1007/s11265-007-0067-4Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology, 57, 758–71.
http://dx.doi.org/10.1080/10635150802429642Stock, S.P., Campbell, J.F. & Nadler, S.A. (2001) Phylogeny of Steinernema Travassos, 1927 (Cephalobina: Steinernematidae) inferred from ribosomal DNA sequences and morphological characters. Journal of Parasitology, 87, 877–889.
http://dx.doi.org/10.1645/0022–3395Surber, E.W. (1928) Megalogonia ictaluri, a new species of trematode from the channel cat-fish, Ictalurus punctatus. Journal of Parasitology, 14, 269–269.
http://dx.doi.org/10.2307/3271386Swofford, D.L. (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.
Szidat, L. (1954) Trematodes nuevos de peces de agua dulce de la República Argentina y un intento para aclarar su carácter marino. Revista del Instituto de Investigación de las Ciencias Naturales y Museo Argentino de Ciencias Naturales ‘‘Bernardino Rivadavia’’, 3, 1–85.
Thompson, J., Gibson, T., Plewnlak, F., Jeanmougin, F. & Higgins, D. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876–4882.
http://dx.doi.org/10.1093/nar/25.24.4876Tkach, V.V. & Curran, S.S. (2015) Prosthenystera oonastica n. sp. (Digenea: Callodistomidae) from ictalurid catfishes in southeastern United States and molecular evidence differentiating species in the genus across Americas. Systematic Parasitology, 90, 39–51.
http://dx.doi.org/10.1007/s11230-014-9531-2Travassos, L. (1922) Contribuições para o conhecimento da fauna helmintológica brasileira - XIV. Espécies brasileiras da família Gorgoderidae Looss, 1901. Brasil Médico, 36 , 17–20.
Tsimbaliuk, A.K. & Roitman, V.A. (1966) Trematode Bunodera mediovitellata parasite of stickleback in Commodore Islands. Trudy Gel'mint. Lab., Akad Nauk SSSR, 17, 290–296.
Van Cleave, H.J. & Mueller, J.E (1932) Parasites of Oneida Lake Fishes. Part I. Description of new genera and new species. Roosevelt Wild Life Annals, 3, 5–71.
Wallin, I.E. (1909) A new species of the trematode genus Allocreadium, with a revision of the genus and a key to the sub-familyAllocreadiinae. Transactions of the American Microscopical Society, 29, 50–66.
http://dx.doi.org/10.2307/3220971