During a survey on the myxosporean fauna of Rajiformes from the Atlantic coast of Argentina, in waters off Buenos Aires Province (34°-42°S; 53°-62°W), the gall bladders of 217 specimens belonging to seven species of skates, representatives of two families, were examined. As a result, three species of Chloromyxum Mingazzini, 1890, namely C. atlantoraji n. sp., C. zearaji n. sp. and C. riorajum Azevedo, Casal, Garcia, Matos, Teles-Grilo and Matos, 2009 were found infecting three endemic host species, the spotback skate Atlantoraja castelnaui (Arhynchobatidae), the yellownose skate Zearaja chilensis (Rajidae) and the Rio skate Rioraja agassizii (Arhynchobatidae), respectively. These species were described based on myxospore morphology and morphometry characterization, as well as by providing their small subunit ribosomal DNA (SSU rDNA) sequences. The SSU rDNA-based phylogenetic analyses showed that these three species constituted a well-established monophyletic subclade within the marine Chloromyxum clade, while branches subtending the other Chloromyxum species were poorly resolved or unresolved, independently of the host taxonomic identities (Carchariniformes, Myliobatiformes, Orectolobiformes, Pristiophoriformes, Rajiformes, Squaliformes and Torpediniformes) and/or host geographic distribution (Atlantic coast of Portugal, Atlantic coast of the USA, Australian waters or Mediterranean Sea). The possible causes of these discrepancies are discussed, providing new insights into the phylogeny of the marine Chloromyxum clade.

Lors d’une étude de la faune des Myxozoaires des Rajiformes de la côte atlantique argentine, dans les eaux situées au large de la province de Buenos Aires (34°–42°S; 53°–62°O), les vésicules biliaires de 217 spécimens appartenant à sept espèces, représentants deux familles, ont été examinés. En conséquence, trois espèces de Chloromyxum Mingazzini, 1890, à savoir C. atlantoraji n. sp., C. zearaji n. sp. et C. riorajum Azevedo, Casal, Garcia, Matos, Teles-Grilo et Matos, 2009 ont été trouvées, infectant trois espèces hôtes endémiques, Atlantoraja castelnaui (Arhynchobatidae), Zearaja chilensis (Rajidae) et Rioraja agassizii (Arhynchobatidae), respectivement. Ces espèces sont décrites sur la base de la morphologie et de la morphométrie des myxospores, ainsi qu’en fournissant leurs petites séquences d’ADN ribosomal (SSU ADNr). Les analyses phylogénétiques basées sur l’ADNr SSU ont montré que ces trois espèces constituaient un sous-clade monophylétique bien établi dans le clade des Chloromyxum marins, tandis que les branches sous-jacentes aux autres espèces de Chloromyxum étaient mal ou non résolues, indépendamment des identités taxonomiques hôtes (Carchariniformes, Myliobatiformes, Orectolobiformes, Pristiophoriformes, Rajiformes, Squaliformes et Torpediniformes) et/ou de la répartition géographique de l’hôte (côte atlantique du Portugal, côte atlantique des États-Unis, eaux australiennes ou mer Méditerranée). Les causes possibles de ces divergences sont discutées, fournissant de nouvelles informations sur la phylogénie du clade des Chloromyxum marins.

Institute of Parasitology Biology Centre of the Czech Academy of Sciences Branišovská 31 37005 České Budějovice Czech Republic

Laboratorio de Ictioparasitología Instituto de Investigaciones Marinas y Costeras Universidad Nacional de Mar del Plata Mar del Plata Argentina

See more in PubMed

Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46.

Anderson MJ, Robinson J. 2003. Generalized discriminant analysis based on distances. Australian & New Zealand Journal of Statistics, 45, 301–318.

Anderson MJ, Willis TJ. 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology, 84, 511–525.

Anderson MJ, Gorley RN, Clarke KR. 2008. PERMANOVA + for PRIMER: Guide to Software and Statistical Methods. PRIMER-E Ltd.: Plymouth.

Asahida T, Kobayashi T, Saitoh K, Nakayama I. 1996. Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentration of urea. Fisheries Science, 62, 727–730.

Atkinson SD, Bartošová-Sojková P, Whipps CM, Bartholomew JL. 2015. Approaches for characterising Myxozoan species, in Myxozoan evolution, ecology and development. Okamura B, Gruhl A, Bartholomew JL, Editors. Springer: London: p. 111–123.

Awerinzew S. 1913. Ergebnisse der Intersuchungen über parasitische Protozoen der tropischen Region Afrikas. Zoologischer Anzeiger, 42, 151–156.

Azevedo C, Casal G, García P, Matos P, Teles-Grilo L, Matos E. 2009. Ultrastructural and phylogenetic data of Chloromyxum riorajum sp. nov. (Myxozoa), a parasite of the stingray Rioraja agassizii in Southern Brazil. Diseases of Aquatic Organisms, 85, 41–51. PubMed

Barker SC. 1991. Evolution of host-parasite associations among species of lice and rock wallabies: coevolution? International Journal for Parasitology, 21, 497–501. PubMed

Barraclough TG, Nee S. 2001. Phylogenetics and speciation. Trends in Ecology & Evolution, 16, 391–399. PubMed

Barta JR, Martin DS, Liberator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD, Profous-Juchelka H. 1997. Phylogenetic relationship among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology, 83, 262–271. PubMed

Bartošová P, Fiala I. 2011. Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa). Parasitology Research, 108, 573–583. PubMed

Bartošová P, Fiala I, Hypša V. 2009. Concatened SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxozporea) and provide an effective tool for their molecular phylogenetics. Molecular Phylogenetics and Evolution, 53, 81–93. PubMed

Bartošová P, Fiala I, Jirků M, Cinková M, Caffara M, Fioravanti ML, Atkinson SD, Bartholomew JL, Holzer AS. 2013. Sphaerospora sensu stricto: Taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa). Molecular Phylogenetics and Evolution, 68, 93–105. PubMed

Bergsten J. 2005. A review of long-branch attraction. Cladistics, 21, 163–193. PubMed

Boeger WA, Kritsky DC. 1997. Coevolution of the Monogenoidea (Platyhelminthes) based on a revised hypothesis of parasite phylogeny. International Journal for Parasitology, 27, 1495–1511. PubMed

Brooks DR, McLennan DA. 1993. Parascript – Parasites and the language of evolution. Smithsonian Institution Press: Washington, DC.

Clarke KR, Gorley RN. 2015. PRIMER v7: User Manual/Tutorial. PRIMER-E Ltd.: Plymouth.

Clarke KR, Gorley RN, Somerfield PJ, Warwick RM. 2014. Change in marine communities. An approach to statistical analysis and interpretation. PRIMER-E Ltd.: Plymouth.

Colonello JH, Cortés F, Massa AM. 2014. Species richness and reproductive modes of chondrichthyans in relation to temperature and fishing effort in the Southwestern Atlantic Shelf (34–54° S). Fisheries Research, 160, 8–17.

Cribb TH, Bray RA, Littlewood DTJ. 2001. The nature and evolution of the association among digeneans, molluscs and fishes. International Journal for Parasitology, 31, 997–1011. PubMed

Díaz de Astarloa JM, Mabragaña E, Hanner E, Figueroa DE. 2008. Morphological and molecular evidence for a new species of longnose skate (Rajiformes: Rajidae: Dipturus) from Argentinean waters based on DNA barcoding. Zootaxa, 1924, 35–46.

Eagles G. 2007. New angles on south Atlantic opening. Geophysical Journal International, 168, 353–361.

Ebert DA, Compagno LJV. 2007. Biodiversity and systematic of skates (Chondrichthyes: Rajiformes: Rajoidei). Environmental Biology of Fishes, 80, 111–124.

Eiras JC, Lu YS, Gibson DI, Fiala I, Saraiva A, Cruz C, Santos MJ. 2012. Synopsis of the species Chloromyxum Mingazinni, 1890 (Myxozoa: Myxosporea: Chloromyxidae). Systematic Parasitology, 83, 203–225. PubMed

Eschmeyer WN, Fricke R, van der Laan R. 2016. Catalog of fishes: genera, species, references. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed 1 August 2017.

Evdokimova EB. 1977. Myxosporidians of teleost fishes from the Patagonian shelf (The Atlantic Coast of Argentina). Parazitologiya, 11, 166–178. PubMed

Fiala I. 2006. The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology, 36, 1521–1534. PubMed

Fiala I, Bartošová P. 2010. History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evolutionary Biology, 10, 228. PubMed PMC

Fiala I, Dyková I. 2004. The phylogeny of marine and freshwater species of the genus Chloromyxum Mingazzini, 1890 (Myxosporea: Bivalvulida) based on small subunit ribosomal RNA gene sequences. Folia Parasitologica, 51, 211–214. PubMed

Fiala I, Bartošová-Sojková P, Whipps CM. 2015. Classification and phylogenetics of Myxozoa, in Myxozoan evolution, ecology and development. Okamura B, Gruhl A, Bartholomew JL, Editors. Springer: London: p. 85–110.

Figueroa DE, Barbini S, Scenna L, Belleggia M, Delpiani G, Spath C. 2013. El endemismo en las rayas de la Zona Común de Pesca Argentino-Uruguaya. Frente Marítimo, 23, 95–104.

Froese R, Pauly D. 2016. FishBase. World Wide Web electronic publication. http://fishbase.org. Accessed 1 August 2017.

Gioia I, Cordeiro NS. 1996. Brazilian myxosporidians’ checklist (Myxozoa). Acta Protozoologica, 35, 137–149.

Gleeson RJ, Adlard RD. 2012. Phylogenetic relationship amongst Chloromyxum Mingazzini, 1890 (Myxozoa: Myxosporea), and the description of six novel species from Australian elasmobranchs. Parasitology International, 61, 267–274. PubMed

Hallet SL, Diamant A. 2001. Ultrastructure and small-subunit ribosomal DNA sequence of Henneguya lesteri n. sp. (Myxosporea), a parasite of sand whiting Sillago analis (Sillaginidae) from the coast of Queensland, Australia. Diseases of Aquatic Organisms, 46, 197–212. PubMed

Hoberg EP, Brooks DR. 2008. A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems. Journal of Biogeography, 35, 1533–1550.

Hoberg EP, Klassen GJ. 2002. Revealing the faunal tapestry: co-evolution and historical biogeography of hosts and parasites in marine systems. Parasitology, 124, S3–S22. PubMed

Hoberg EP, Brooks DR, Siegel-Causey D. 1997. Host–parasite cospeciation: history, principles and prospects, in Host–parasite evolution: General principles and avian models. Clayton DH, Moore J, Editors. Oxford University Press: Oxford: p. 212–235.

Hoberg EP, Gardner SL, Campbell RA. 1999. Systematics of the Eucestoda: advances toward a new phylogenetic paradigm, and observations on the early diversification of tapeworms and vertebrates. Systematic Parasitology, 42, 1–12. PubMed

Holzer AS, Sommerville C, Wootten R. 2004. Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. International Journal for Parasitology, 34, 1099–1111. PubMed

Holzer AS, Wootten R, Sommerville C. 2010. Zschokkella hildae Auerbach, 1910: Phylogenetic position, morphology, and location in cultured Atlantic cod. Parasitology International, 59, 133–140. PubMed

Humphries EM, Winker K. 2010. Working through polytomies: Auklets revisited. Molecular Phylogenetics and Evolution, 54, 88–96. PubMed

Jameson AP. 1929. Myxosporidia from Californian fishes. Journal of Parasitology, 16, 59–68.

Jaureguizar AJ, Menni RC, Lasta CA, Guerrero RA. 2006. Fish assemblages of the northern Argentine coastal system: spatial patterns and their temporal variations. Fisheries Oceanography, 15, 326–344.

Jirků M, Fiala I, Modrý D. 2007. Tracing the genus Sphaerospora: rediscovery, redescription and phylogeny of the Sphaerospora ranae (Morelle, 1929) n. comb. (Myxosporea, Sphaerosporidae), with emendation of the genus Sphaerospora. Parasitology, 134, 1727–1739. PubMed

Jirků M, Bartošová P, Kodádková A, Mutschmann F. 2011. Another chloromyxid lineage: molecular phylogeny and redescription of Chloromyxum careni from the Asian Horned frog Megophrys nasuta. Journal of Eukaryotic Microbiology, 58, 50–59. PubMed

Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acid Research, 30, 3059–3066. PubMed PMC

Kent ML, Khattra J, Hervio DML, Devlin RH. 1998. Ribosomal DNA sequence analysis of isolates of the PKX myxosporean and their relationship to members of the genus Sphaerospora. Journal of Aquatic Animal Health, 10, 12–21.

Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao C. 2001. Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology, 48, 395–413. PubMed

Kodádková A, Bartošová-Sojková P, Holzer AS, Fiala I. 2015. Bipteria vetusta n. sp. – an old parasite in an old host: tracing the origin of myxosporean parasitism in vertebrates. International Journal for Parasitology, 45, 269–276. PubMed

Kovaljova AA. 1988. Myxoporidia of the genus Chloromyxum (Cnidospora, Myxosporea) of cartilaginous fishes from the Atlantic coast of Africa. Parazitologiya, 22, 384–388.

Kudo RR. 1919. Studies on Myxosporidia. A synopsis on genera and species of Myxosporidia. Biological Monographs, 5, 1–265.

Kuznetsova IG. 1977. Myxosporidians of Chondrostei from the Patagonian shelf. Parazitologiya, 11, 74–77. PubMed

Lom J, Arthur JR. 1989. A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases, 12, 151–156.

Lom J, Dyková I. 1992. Protozoan Parasites of Fishes. Developments in Aquaculture and Fisheries. Elsevier: Amsterdam.

Lom J, Dyková I. 2006. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica, 53, 1–36. PubMed

Lucifora LO, García VB, Menni RC, Worm B. 2012. Spatial patterns in the diversity of sharks, rays, and chimaeras (Chondrichthyes) in the Southwest Atlantic. Biodiversity and Conservation, 21, 407–419.

Menni RC, López HL. 1984. Distributional patterns of Argentine marine fishes. Physis, 42, 71–85.

Menni RC, Lucífora LO. 2007. Condrictios de la Argentina y Uruguay. Lista de Trabajo. ProBiota, FCNyM, UNLP, Serie Técnica-Didactica, La Plata, Argentina, 11, 1–15.

Menni RC, Stehmann MF. 2000. Distribution, environment and biology of batoid fishes off Argentina, Uruguay and Brazil. A review. Revista del Musea Argentino de Ciencias Naturales (Argentina), 2, 69–109.

Menni RC, Rincón G, García ML. 2008. Discopyge castelloi sp. nov. (Torpediniformes, Narcinidae), una nueva especie de raya eléctrica del Mar Argentina. Revista del Musea Argentino de Ciencias Naturales (Argentina), 10, 161–171.

Menni RC, Jaureguizar AJ, Stehmann MFW, Lucifora LO. 2010. Marine biodiversity at the community level: zoogeography of sharks, skates, rays and chimaeras in the Southwestern Atlantic. Biodiversity and Conservation, 19, 775–796.

Mingazzini P. 1890. Sullo sviluppo dei Myxosporidi. Bollettino della Società di Naturalisti, 4, 160–164.

Molnár K. 1994. Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitologica Hungarica, 27, 5–20.

Molnár K, Eszterbauer E. 2015. Specificity of infection sites in vertebrate hosts, in Myxozoan evolution, ecology and development. Okamura B, Gruhl A, Bartholomew JL, Editors. Springer: London: p. 295–313.

Morand S, Guégan J-F. 2000. Patterns of endemism in host-parasite associations: lessons from epidemiological models and comparative test. Belgian Journal of Entomology, 2, 135–147.

Paterson AM, Banks J. 2001. Analytical approaches to measuring co-speciation of host and parasites: through the glass darkly. International Journal for Parasitology, 31, 1012–1022. PubMed

Pinto C. 1928. Mixosporídeos e outros protozoários intestinais observados na América do Sul. Archivos do Instituto Biológico, 1, 101–102.

Rambaut A, Drummond AJ. 2007. Tracer v1.4 http://beast.bio.ed.ac.uk/Tracer

Rocha S, Azevedo C. 2012. Light and electron microscopy applied to the characterization of marine species belonging to the genus Chloromyxum, as a study model for myxosporean parasites, in Current Microscopy Contributions to Advances in Science and Technology, Méndez-Vilas A, Editor.Formatex Research Center: Badajoz, p. 471–477.

Rocha S, Casal G, Al-Quraishy S, Azevedo C. 2013. Morphological and molecular characterization of a new myxozoan species (Myxosporea) infecting the gall bladder of Raja clavata (Chondrichthyes), from the Portuguese Atlantic Coast. Journal of Parasitology, 99, 307–317. PubMed

Rocha S, Casal G, Al-Quraishy S, Azevedo C. 2014. Morphological and ultrastructural redescription of Chloromyxum leydigi Mingazzini, 1890 (Myxozoa: Myxosporea), type species of the genus, infecting the gall bladder of the marine cartilaginous fish Torpedo marmorata Risso (Chondrichthyes: Torpedinidae), from the Portuguese Atlantic coast. Folia Parasitologica, 61, 1–10. PubMed

Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. PubMed

Ruocco NL, Lucifora LO, Díaz de Astarloa JM, Mabragaña EM, Delpiani MS. 2012. Morphology and DNA barcoding reveal a new species of eagle ray from the Southwestern Atlantic: Myliobatis ridens sp. nov. (Chondrichthyes: Myliobatiformes: Myliobatidae). Zoological Studies, 51, 863–873.

Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675. PubMed PMC

Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690. PubMed

Swofford DL. 2003. PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.

Intraspecific Morphometric Variation in a New Species of Ceratomyxa Thélohan 1892 (Cnidaria) from the South Atlantic Ocean: An Ecomorphological Study Using Geometric Morphometrics

Unraveling the mystery of a myxozoan parasite of the trout: redescription of Chloromyxum schurovi

Mechanisms and Drivers for the Establishment of Life Cycle Complexity in Myxozoan Parasites

Morphological and molecular-genetic characterization of Chloromyxum trilineatum n. sp. (Myxosporea: Bivalvulida) in the gall bladder of pale chub (Zacco platypus) in Japan