Advertisement

Diversity of Empruthotrema Johnston and Tiegs, 1992 parasitizing batoids (Chondrichthyes: Rajiformes and Myliobatiformes) from the Southwest Atlantic Ocean, with description of three new species

  • Manuel M. IrigoitiaEmail author
  • Paola E. Braicovich
  • María A. Rossin
  • Delfina Canel
  • Eugenia Levy
  • Marisa D. Farber
  • Juan T. Timi
Fish Parasitology - Original Paper

Abstract

During an extensive research project involving 519 specimens of batoids, including 13 species of Rajiformes and Myliobatiformes (Chondrichthyes) from the Argentine Sea, three new species of Empruthotrema were found and are described using morphologic characteristics and two molecular markers: LSU rDNA and COI mtDNA. The new species can be distinguished from their congeners by the number and distribution of the marginal loculi, the length and morphology of male copulatory organ, and the presence of eyespots. Additionally, multivariate analysis identified the dimensions of the pharynx and ejaculatory bulb as diagnostic features. Host specificity and previous records of the genus in the region are discussed. This is the first description of new species in this genus for the Southwestern Atlantic Ocean, as well as for arhynchobatid hosts.

Keywords

Empruthotrema aoneken Empruthotrema orashken Empruthotrema dorae Rajiformes Myliobatiformes Argentine Sea 

Notes

Acknowledgments

Thanks are extended to Dr. Aneta Yoneva from the Institute of Biodiversity and Ecosystem Research (Sofia, Bulgaria) for translating Russian literature. To Dr. Ana Fernandez Garay from the Instituto de Lingüística y Letras UBA-CONICET (Argentina) for her help with Tehuelche native language. To Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP) and Industrias El Corsario A.A. (Mar del Plata, Argentina), for providing fish samples. To Dr. Santiago Barbini, Dr. David Sabadin, Lic. Jorge Roman, Lic. Melisa Chierichietti and Dr. Lorena Scenna (IIMyC-CONICET) for helping with fish identification and sample collection.

Funding information

Financial support provided by grants from Consejo Nacional de Investigaciones Científicas y Técnicas (PIP No. 112-201501-00973), Fondo para la Investigación Científica y Tecnológica (PICT 2015 No. 2013) and Universidad Nacional de Mar del Plata (EXA 915/18).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410.  https://doi.org/10.1016/S0022-2836(05)80360-2 CrossRefGoogle Scholar
  2. Álvarez MF, Aragort W, Leiro JM, Sanmartín ML (2006) Macroparasites of five species of ray (genus Raja) on the northwest coast of Spain. Dis Aquat Org 70:93–100.  https://doi.org/10.3354/dao070093 CrossRefGoogle Scholar
  3. Anderson MJ, Robinson J (2003) Generalized discriminant analysis based on distances. Aust N Z J Stat 45:301–318.  https://doi.org/10.1111/1467-842X.00285 CrossRefGoogle Scholar
  4. Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525.  https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2 CrossRefGoogle Scholar
  5. Anderson MJ, Gorley RN, Clarke RK (2008) Permanova+ for primer: guide to software and statistical methods. Primer-E Limited, Plymouth, UKGoogle Scholar
  6. Chisholm LA, Whittington ID (1999) A revision of the Merizocotylinae Johnston and Tiegs, 1922 (Monogenea: Monocotylidae) with descriptions of new species of Empruthotrema Johnston and Tiegs, 1922 and Merizocotyle Cerfontaine, 1894. J Nat Hist 33:1–28.  https://doi.org/10.1080/002229399300452 CrossRefGoogle Scholar
  7. Chisholm LA, Whittington ID (2005) Empruthotrema stenophallus n. sp. (Monogenea: Monocotylidae) from the nasal tissue of Dasyatis kuhlii (Dasyatidae) from Sabah, Borneo, Malaysia. J Parasitol 91:522–526.  https://doi.org/10.1645/GE-3458 CrossRefGoogle Scholar
  8. Chisholm LA, Wheeler TA, Beverley-Burton M (1995) A phylogenetic analysis and revised classification of the Monocotylidae Taschenberg, 1879 (Monogenea). Syst Parasitol 32:159–191.  https://doi.org/10.1007/BF00008827 CrossRefGoogle Scholar
  9. Chisholm LA, Hansknecht TJ, Whittington ID, Overstreet RM (1997) A revision of the Calicotylinae Monticelli, 1903 (Monogenea: Monocotylidae). Syst Parasitol 38:159–183.  https://doi.org/10.1023/A:1005844306178 CrossRefGoogle Scholar
  10. Chisholm LA, Morgan JAT, Adlard RD, Whittington ID (2001) Phylogenetic analysis of the Monocotylidae (Monogenea) inferred from 28S rDNA sequences. Int J Parasitol 31:1253–1263.  https://doi.org/10.1016/S0020-7519(01)00223-5 CrossRefGoogle Scholar
  11. Cousseau MB, Perrotta RG (2013) Peces marinos de Argentina: biología, distribución, pesca. Instituto Nacional de Investigación y Desarrollo Pesquero INIDEP, Mar del Plata, Argentina.Google Scholar
  12. Cousseau MB, Figueroa DE, Díaz de Astarloa JM, Mabragaña E, Lucifora LO (2007) Rayas, chuchos y otros batoideos del Atlántico Sudoccidental (34ºS-55ºS). Instituto Nacional de Investigación y Desarrollo Pesquero INIDEP, Mar del Plata.Google Scholar
  13. Domingues MV, Marques FPL (2007) Revision of Potamotrygonocotyle Mayes, Brooks & Thorson, 1981 (Platyhelminthes: Monogenoidea: Monocotylidae), with descriptions of four new species from the gills of the freshwater stingrays Potamotrygon spp. (Rajiformes: Potamotrygonidae) from the La Plata river basin. Syst Parasitol 67:157–174.  https://doi.org/10.1007/s11230-006-9086-y
  14. Dzika E (2002) Deformations of the attachment organ in Diplozoidae (Palombi, 1949) (Monogenea). Wiad Parazytol 48:69–77Google Scholar
  15. Ebert DA, Compagno LJV (2007) Biodiversity and systematics of skates (Chondrichthyes: Rajiformes: Rajoidei). In: Biology of skates. Springer, Dordrecht, pp 5–18Google Scholar
  16. Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319.  https://doi.org/10.1111/j.1096-0031.1994.tb00181.x CrossRefGoogle Scholar
  17. Fehlauer-Ale KH, Littlewood DTJ (2011) Molecular phylogeny of Potamotrygonocotyle (Monogenea, Monocotylidae) challenges the validity of some of its species. Zool Scr 40:638–658.  https://doi.org/10.1111/j.1463-6409.2011.00496.x CrossRefGoogle Scholar
  18. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791.  https://doi.org/10.1111/j.1558-5646.1985.tb00420.x CrossRefGoogle Scholar
  19. Figueroa DE, Barbini SA, Scenna LB, Bellegia M, Delpiani GE, Spath MC (2013) El endemismo en las rayas de la Zona Común de Pesca Argentino-Uruguaya. Frent Mar 23:95–104Google Scholar
  20. Filatov DA (2002) Proseq: a software for preparation and evolutionary analysis of DNA sequence data sets. Mol Ecol Notes 2:621–624.  https://doi.org/10.1046/j.1471-8286.2002.00313.x CrossRefGoogle Scholar
  21. Fricke R, Eschmeyer WN, van der Laan R (2018) Catalog of fishes: genera, species, reference. Cat. Fishes http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Accessed 18 Sep 2018
  22. Froese R, Pauly D (2018) FishBase. World Wide Web electronic publication https://www.fishbase.de/. Accessed 1 Mar 2019
  23. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704.  https://doi.org/10.1080/10635150390235520 CrossRefGoogle Scholar
  24. Hassouna N, Mithot B, Bachellerie J-P (1984) The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res 12:3563–3583.  https://doi.org/10.1093/nar/12.8.3563 CrossRefGoogle Scholar
  25. Hebert PDN, Ratnasingham S, deWaard JR (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B Biol Sci 270:S96–S99.  https://doi.org/10.1098/rsbl.2003.0025 Google Scholar
  26. Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192.  https://doi.org/10.1093/sysbio/42.2.182 CrossRefGoogle Scholar
  27. Irigoitia MM, Cantatore DMP, Delpiani GE, Incorvaia IS, Lanfranchi AL, Timi JT (2014) Merizocotyle euzeti sp. n. (Monogenea: Monocotylidae) from the nasal tissue of three deep sea skates (Rajidae) in the southwestern Atlantic Ocean. Folia Parasitol (Praha) 61:206–212.  https://doi.org/10.14411/fp.2014.031 CrossRefGoogle Scholar
  28. Irigoitia MM, Incorvaia IS, Timi JT (2017) Evaluating the usefulness of natural tags for host population structure in chondrichthyans: parasite assemblages of Sympterygia bonapartii (Rajiformes: Arhynchobatidae) in the southwestern Atlantic. Fish Res 195:80–90.  https://doi.org/10.1016/j.fishres.2017.07.006 CrossRefGoogle Scholar
  29. Kritsky DC, Bullard SA, Ruiz CF, Warren MB (2017) Empruthotrema longipenis n. sp. (Monogenoidea: Monocotylidae: Merizocotylinae) from the olfactory sacs of the smooth butterfly ray Gymnura micrura (Bloch & Schneider) (Myliobatiformes: Gymnuridae) in the Gulf of Mexico. Syst Parasitol 94:777–784.  https://doi.org/10.1007/s11230-017-9741-5 CrossRefGoogle Scholar
  30. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefGoogle Scholar
  31. Kuznetsova IG (1975) Monogenea from Chondrichthyes fish of the Patagonian shelf. Ekol Eksp Parazitol 1:143–153 (in Russian) Google Scholar
  32. Littlewood DTJ, Rohde K, Clough KA (1997) Parasite speciation within or between host species?—phylogenetic evidence from site-specific polystome monogeneans. Int J Parasitol 27:1289–1297.  https://doi.org/10.1016/S0020-7519(97)00086-6 CrossRefGoogle Scholar
  33. Lucifora LO, García VB, Menni RC, Worm B (2012) Spatial patterns in the diversity of sharks, rays, and chimaeras (Chondrichthyes) in the Southwest Atlantic. Biodivers Conserv 21:407–419.  https://doi.org/10.1007/s10531-011-0189-7 CrossRefGoogle Scholar
  34. Menni RC, Lucifora L (2007) Condrictios de la Argentina y Uruguay. ProBiota Ser Téc Didáctica 11:1–15Google Scholar
  35. Menni R, Stehmann M (2000) Distribution, environment and biology of batoid fishes off Argentina, Uruguay and Brazil. A review. Rev Mus Argent Cienc Nat Nueva Ser 2:69–109CrossRefGoogle Scholar
  36. Nelson JS, Grande TC, Wilson MVH (2016) Fishes of the world. John Wiley & SonsGoogle Scholar
  37. Pečínková M, Vøllestad LA, Koubková B, Huml J, Jurajda P, Gelnar M (2007) The relationship between developmental instability of gudgeon Gobio gobio and abundance or morphology of its ectoparasite Paradiplozoon homoion (Monogenea). J Fish Biol 71:1358–1370.  https://doi.org/10.1111/j.1095-8649.2007.01599.x CrossRefGoogle Scholar
  38. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256.  https://doi.org/10.1093/molbev/msn083 CrossRefGoogle Scholar
  39. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808.  https://doi.org/10.1080/10635150490522304 CrossRefGoogle Scholar
  40. Poulin R (2002) The evolution of monogenean diversity. Int J Parasitol 32:245–254.  https://doi.org/10.1016/S0020-7519(01)00329-0 CrossRefGoogle Scholar
  41. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574.  https://doi.org/10.1093/bioinformatics/btg180 CrossRefGoogle Scholar
  42. Rossin MA, De Francesco PN, Timi JT (2017) Three-dimensional morphology of rigid structures as a tool for taxonomic studies of Dactylogyridae (Monogenea). Parasitol Res 116:2813–2819.  https://doi.org/10.1007/s00436-017-5591-y CrossRefGoogle Scholar
  43. Ruocco NL, Lucifora LO, de Astarloa JMD, Mabragaña E, Delpiani SM (2012) Morphology and DNA barcoding reveal a new species of eagle ray from the southwestern Atlantic: Myliobatis ridens sp. nov. (Chondrichthyes: Myliobatiformes: Myliobatidae). Zool Stud 51:862–873Google Scholar
  44. Šebelová Š, Kuperman B, Gelnar M (2002) Abnormalities of the attachment clamps of representatives of the family Diplozoidae. J Helminthol 76:249–259.  https://doi.org/10.1079/JOH2002133 CrossRefGoogle Scholar
  45. Swofford DL (2001) PAUP*: phylogenetic analysis using parsimony (and other methods) 40.b5Google Scholar
  46. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526.  https://doi.org/10.1093/oxfordjournals.molbev.a040023 Google Scholar
  47. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680.  https://doi.org/10.1093/nar/22.22.4673 CrossRefGoogle Scholar
  48. Vanhove M, Tessens B, Schoelinck C, Jondelius U, Littlewood T, Artois T, Huyse T (2013) Problematic barcoding in flatworms: a case-study on monogeneans and rhabdocoels (Platyhelminthes). ZooKeys 365:355–379.  https://doi.org/10.3897/zookeys.365.5776 CrossRefGoogle Scholar
  49. Vignon M, Pariselle A, Vanhove MPM (2011) Modularity in attachment organs of African Cichlidogyrus (Platyhelminthes: Monogenea: Ancyrocephalidae) reflects phylogeny rather than host specificity or geographic distribution. Biol J Linn Soc 102:694–706.  https://doi.org/10.1111/j.1095-8312.2010.01607.x CrossRefGoogle Scholar
  50. Whittington ID, Cribb BW, Hamwood TE, Halliday JA (2000) Host-specificity of monogenean (platyhelminth) parasites: a role for anterior adhesive areas? Int J Parasitol 30:305–320.  https://doi.org/10.1016/S0020-7519(00)00006-0 CrossRefGoogle Scholar
  51. Xia X (2018) DAMBE7: new and improved tools for data analysis in molecular biology and evolution. Mol Biol Evol 35:1550–1552.  https://doi.org/10.1093/molbev/msy073 CrossRefGoogle Scholar
  52. Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7.  https://doi.org/10.1016/S1055-7903(02)00326-3 CrossRefGoogle Scholar
  53. Zolovs M, Deksne G, Daukšte J, Aizups Z, Kirjušina M (2016) Morphometric analysis of the hard parts of Pseudodactylogyrus anguillae and Pseudodactylogyrus bini (Monogenea: Dactylogyridae) on the gill apparatus of the European eels (Anguilla anguilla) from the freshwaters of Latvia. J Parasitol 102:388–394.  https://doi.org/10.1645/15-789 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratorio de Ictioparasitología, Facultad de Ciencias Exactas y Naturales, Instituto de Investigaciones Marinas y Costeras (IIMyC)Universidad Nacional de Mar del Plata (UNMdP)Buenos AiresArgentina
  2. 2.Instituto de Biotecnología, Instituto Nacional de Tecnología Agropecuaria (INTA)Buenos AiresArgentina

Personalised recommendations