Skip to main content
SpringerLink
Log in

Molecular Identification of Plerocercoids of Clistobothrium montaukensis (Cestoda: Phyllobothriidea) Parasitizing the King of Herrings Regalecus glesne

  • Short Communication
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Purpose

Endo-parasites of the bathypelagic king of herrings Regalecus glesne and oarfish Regalecus russelii are only known from few specimens opportunistically examined. As a consequence, there are few records of parasites from either Regalecus species. We report plerocercoid larvae of phyllobothriidean cestodes parasitizing an adult R. glesne stranded in Bahía de La Paz, Baja California Sur, Mexico.

Methods

Sixty-three plerocercoids were obtained from the intestine of R. glesne and characterized using morphological and molecular methods (nuclear 28S rDNA and mitochondrial cytochrome c oxidase I gene sequences).

Results

Following the morphological diagnostic criteria of scolex and muscle bands in the strobila, plerocercoids specimens were preliminary assigned to the genus Clistobothrium. Mitochondrial and nuclear DNA sequences indicate these plerocercoids correspond to Clistobothrium montaukensis Ruhnke, 1993.

Conclusion

Regalecus glesne is a new host known for C. montaukensis and this report is a new geographical record of C. montaukensis parasitizing species of the genus Regalecus previously known only from California and Florida, USA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  1. Roberts TR (2002) Payanak as a mythical animal and as the living species Regalecus glesne (Oarfish, Regalecidae, Lampridiformes). Nat Hist Bull Siam Soc 50(2):211–224

    Google Scholar 

  2. Benfield MC, Cook S, Sharuga S, Valentine MM (2013) Five in situ observations of live oarfish Regalecus glesne (Regalecidae) by remotely operated vehicles in the oceanic waters of the northern Gulf of Mexico. J Fish Biol 83:28–38. https://doi.org/10.1111/jfb.12144

    Article  CAS  PubMed  Google Scholar 

  3. Feeney RF, Lea RN (2018) California record of the oarfish, Regalecus russelii (Cuvier, 1816) (Actinopterygii: Regalecidae). Bull South Calif Acad Sci 117:169–179. https://doi.org/10.3160/3294.1

    Article  Google Scholar 

  4. Ahern LAM, Gómez-Gutiérrez J, Aburto-Oropeza O et al (2018) DNA sequencing of fish eggs and larvae reveals high species diversity and seasonal changes in spawning activity in the southeastern Gulf of California. Mar Ecol Prog Ser 592:159–179. https://doi.org/10.3354/meps12446

    Article  CAS  Google Scholar 

  5. Chávez RH, Galván MF, Torres-Villegas JR (1985) Primer registro de Regalecus russelii (Shaw) (Pisces: Regalecidae) de aguas mexicanas. Invest Mar CICIMAR 2:105–112

    Google Scholar 

  6. Castro-Aguirre JL, Arvizu-Martínez J, Alarcón GC (1991) Una especie nueva de Regalecus (Pisces: Lampridiformes) hallada en la Bahía de La Paz, Baja California Sur, México, con notas y observaciones taxonómicas y biogeográficas de la familia Regalecidae. An Esc Nac Cienc Biol Méx 34:159–171

    Google Scholar 

  7. Abitia-Cárdenas LA, Rodríguez-Romero J, Galván-Magaña F et al (1994) Lista sistemática de la ictiofauna de Bahía de la Paz, Baja California Sur, México. Cienc Mar 20:159–181. https://doi.org/10.7773/cm.v20i2.963

    Article  Google Scholar 

  8. Castro-Aguirre JL, Balart EF (1996) Contribución al conocimiento del origen y relaciones de la ictiofauna de aguas profundas del Golfo de California. México Hidrobiológica 6(1–2):67–76

    Google Scholar 

  9. Ramírez-Murillo R, Schmitter-Soto JJ (1996) Un segundo Regalecus kinoi Castro-Aguirre, Arvizu-Martínez and Alarcón-González (Pisces: Regalecidae), hallado en Zihuatanejo, Guerrero, México. Cuad Mex Zool 2:40–43

    Google Scholar 

  10. Balart EF, Castro-Aguirre JL, Amador-Silva E (1999) A new record of the oarfish Regalecus kinoi (Lampridiformes: Regalecidae) in the Gulf of California, Mexico. Oceánides 14:137–140

    Google Scholar 

  11. Hutton RF (1961) A plerocercoid (Cestoda: Tetraphyllidea) from the oar-fish, Regalecus glesne (Ascanius), with notes on the biology of the oar-fish. Bull Mar Sci Gulf Caribb 11(2):309–317

    Google Scholar 

  12. Villarreal LA, Dailey MD (1993) Syncoelium regaleci sp. n. (Digenea: Syncoeliidae) from the branchial cavity of the oarfish (Regalecus glesne). J Helminthol Soc Wash 60:162–164

    Google Scholar 

  13. Kuris A, Jaramillo AG, McLaughlin JP et al (2015) Monsters of the sea serpent: parasites of an oarfish, Regalecus russellii. J Parasitol 101:41–44. https://doi.org/10.1645/14-581.1

    Article  PubMed  Google Scholar 

  14. Lozano-Cobo H, Gómez del Prado-Rosas MC, Sánchez-Velasco L, Gómez-Gutiérrez J (2017) Seasonal variation in chaetognath and parasite species assemblages along the northeastern coast of the Yucatan Peninsula. Dis Aquat Org 124:55–71. https://doi.org/10.3354/dao03106

    Article  Google Scholar 

  15. Salgado-Madonado G (1979) Procedimientos y técnicas generales empleados en los estudios helmintológicos. Laboratorio de helmintología, Oficina de sanidad, nutrición y genética, Dirección General de Acuacultura, Departamento de Pesca, Mexico City

  16. Ruhnke TR (2011) A monograph on the Phyllobothriidae (Platyhelminthes: Cestoda). Bull Univ Nebraska St Mus 25:1–205

    Google Scholar 

  17. Lozano-Cobo H, Gómez-Gutiérrez J, Franco-Gordo C, Gómez del Prado-Rosas MC (2017) The discovery of acanthocephalans parasitizing chaetognaths. Acta Parasitol 62:401–411. https://doi.org/10.1515/ap-2017-0048

    Article  CAS  PubMed  Google Scholar 

  18. Chervy L (2002) The terminology of larval cestodes or metacestodes. Syst Parasitol 52:1–33. https://doi.org/10.1023/A:1015086301717

    Article  Google Scholar 

  19. Ivanova NV, Dewaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6:998–1002. https://doi.org/10.1111/j.1471-8286.2006.01428.x

    Article  CAS  Google Scholar 

  20. Bowles J, Blair D, Mcmanus DP (1992) Genetic variants within the genus Echinococcus identified by mitocondrial DNA sequencing. Mol Biochem Parasit 54:165–173

    Article  CAS  Google Scholar 

  21. Miura O, Kuris AM, Torchin ME et al (2005) Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). Int J Parasitol 35:793–801. https://doi.org/10.1016/j.ijpara.2005.02.014

    Article  CAS  PubMed  Google Scholar 

  22. Van der Auwera G, Chapelle S, De Wächter R (1994) Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of the omycetes. FEBS Lett 338:133–136

    Article  PubMed  Google Scholar 

  23. Tkach V, Pawlowski J (1999) A method of DNA extraction from the etanol-fixed parasitic worms. Acta Parasitol 44:147–178

    CAS  Google Scholar 

  24. Littlewood DTJ, Curini-Galleti M, Herniou AE (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol Phylogenet Evol 16:449–466. https://doi.org/10.1006/mpev.2000.0802

    Article  CAS  PubMed  Google Scholar 

  25. Littlewood DTJ, Waeschenbach A, Nikolov PN (2008) In search of mitochondrial markers for resolving the phylogeny of cyclophyllidean tapeworms (Platyhelminthes, Cestoda)—a test study with Davaineidae. Acta Parasitol 53(2):133–144. https://doi.org/10.2478/s11686-008-0029-4

    Article  CAS  Google Scholar 

  26. Reyda FB, Olson PD (2003) Cestodes of Peruvian freshwater stingrays. J Parasitol 89:1018–1024. https://doi.org/10.1645/GE-3143

    Article  CAS  PubMed  Google Scholar 

  27. Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  28. Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    Article  CAS  PubMed  Google Scholar 

  29. Caira JN, Jensen K, Waeschenbach A et al (2014) Orders out of chaos—molecular phylogenetics reveals the complexity of shark and stingray tapeworm relationships. Int J Parasitol 44:55–73. https://doi.org/10.1016/j.jipara.2013.10.004

    Article  CAS  PubMed  Google Scholar 

  30. Caira JN, Jensen K, Hayes C, Ruhnke TR (2020) Insights from new cestodes of the crocodile shark, Pseudocarcharias kamoharai (Lamniformes: Pseudocarchariidae), prompt expansion of Scyphophyllidium and formal synonymization of seven phyllobothriidean genera—at last! J Helminthol 94:e132. https://doi.org/10.1017/S0022149X20000036

    Article  CAS  PubMed  Google Scholar 

  31. Caira JN, Jensen K, Pickering M et al (2020) Intrigue surrounding the life-cycles of species of Clistobothrium (Cestoda: Phyllobothriidea) parasitising large pelagic sharks. Int J Parasitol 50(13):1043–1055. https://doi.org/10.1016/j.ijpara.2020.08.002

    Article  CAS  PubMed  Google Scholar 

  32. de Chambrier A, Brabec J, Tran BT, Scholz T (2019) Revision of Acanthotaenia von Linstow, 1903 (Cestoda: Proteocephalidae), parasites of monitors (Varanus spp.), based on morphological and molecular data. Parasitol Res 118(6):1761–1783. https://doi.org/10.1007/s00436-019-06326-6

    Article  PubMed  Google Scholar 

  33. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ruhnke TR (1993) A new species of Clistobothrium (Cestoda: Tetraphyllidea), with an evaluation of the systematic status of the genus. J Parasitol 79:37–43. https://doi.org/10.2307/3283274

    Article  Google Scholar 

  35. Guardone L, Giusti A, Bilska-Zajac E et al (2020) Molecular characterization of Clistobothrium sp. viable plerocercoids in fresh longfin inshore squid (Doryteuthis pealeii) and implications for cephalopod inspection. Pathogens 9(7):1–17. https://doi.org/10.3390/pathogens9070596

    Article  CAS  Google Scholar 

  36. Waeschenbach A, Webster BL, Littlewood DTJ (2012) Adding resolution to ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with large fragments of mtDNA. Mol Phylogenet Evol 63:834–847. https://doi.org/10.1016/j.ympev.2012.02.020

    Article  CAS  PubMed  Google Scholar 

  37. Ruhnke TR, Caira JN, Pickering M (2017) 16 Phyllobothriidea Caira, Jensen, Waeschenbach, Olson & Littlewood, 2014. In: Caira JN, Jensen K (eds) Planetary biodiversity inventory (2008–2017): tapeworms from vertebrate bowels of the earth. University of Kansas, Natural History Museum, Special Publication No. 25, Lawrence, KS, USA, pp 305–326

    Google Scholar 

  38. Caira JN, Jensen K (2017) Planetary biodiversity inventory (2008–2017): tapeworms from vertebrate bowels of the earth. University of Kansas, Natural History Museum, Special Publication No. 25, Lawrence, KS, USA, p 464

    Google Scholar 

  39. Pardo-Gandarillas MC, Lohrmann KB, Valdivia AL, Ibañez CM (2009) First record of parasites of Dosidicus gigas (d’Orbigny, 1835) (Cephalopoda: Ommastrephidae) from the Humboldt Current system off Chile. Rev Biol Mar Oceanogr 44:397–408. https://doi.org/10.4067/S0718-19572009000200013

    Article  Google Scholar 

  40. Brickle P, Olson PD, Littlewood DT et al (2001) Parasites of Loligo gahi from waters off the Falkland Islands, with a phylogenetically based identification of their cestode larvae. Can J Zool 79:2289–2296. https://doi.org/10.1139/z01-189

    Article  Google Scholar 

  41. Randhawa HS, Brickle P (2011) Larval parasite gene sequence data reveal cryptic trophic links in life cycles of porbeagle shark tapeworms. Mar Ecol Prog Ser 431:215–222. https://doi.org/10.3354/meps09108

    Article  Google Scholar 

  42. Penadés-Suay J, Tomás J, Merchán M, Aznar FJ (2017) Intestinal helminth fauna of the shortfin mako Isurus oxyrinchus (Elasmobranchii: Lamnidae) in the northeast Atlantic Ocean. Dis Aquat Org 123:45–54. https://doi.org/10.3354/dao03081

    Article  Google Scholar 

  43. Psomadakis P, Bottaro M, Doria G et al (2008) Notes on the Regalecus glesne occurring in the Gulf of Genova and in Liguro-provençal waters (NW Mediterranean) (Pisces, Lampridiformes, Regalecidae). Res Ligusticae 256:549–571

    Google Scholar 

  44. Roberts TR (2012) Systematics, biology, and distribution of the species of the oceanic oarfish genus Regalecus (Teleostei, Lampridiformes, Regalecidae). Mém Mus Natl Hist Nat 202:1–268

    Google Scholar 

Download references

Acknowledgements

We sincerely thank the staff of the Colección Ictiológica del Centro Interdisciplinario de Ciencias Marinas del Instituto Politécnico Nacional (CI-CICIMAR-IPN; http://coleccion.cicimar.ipn.mx/) for allowing us to obtain a sample of the parasites of their dissected R. glesne specimen. We are particularly thankful to José de la Cruz-Agüero for his permission to analyze parasites of this Regalecus specimen. We thank the financial support for the molecular analysis of parasites used in this study provided by the project Zooplankton and their parasites in Los Cabos region (iBOLD Code “ZPCR”). We deeply thank Patricia Cortés-Calva and Griselda Gallegos-Simental (Nodo del Código de Barras de la Vida, MEXBOL at CIBNOR, La Paz, Baja California Sur, Mexico, CONACYT 2017-280896 and 2018-295569) for helping us to extract, amplify and sequence cox1 gene. We also thank Ofelia Delgado, Andrea Jiménez-Marín, Laura Márquez, and Nelly López-Ortíz (Laboratorio Nacional de la Biodiversidad-IB-UNAM) for their valuable assistance with the generation of the nuclear 28S rDNA gene sequences. We also deeply thank Ariel Cruz-Villacorta for his valuable assistance with SEM observations (CIBNOR, La Paz, Baja California Sur, Mexico). We thank to two anonymous referees that greatly improved the present manuscript. This study was partially funded by the projects CONACYT CB-2012-178615-01, CB-2016-01-284201 granted to JG-G; and CONACYT 220408 and PAPIIT IN213520 granted to AO-F. HL-C was supported by a PhD CONACYT (A14618), PIFI-IPN (SIP20110012), and BEIFI-IPN (SIP20140497, 20150113, 20160495, 20171275) grants. All the authors are SNI fellows, and JG-G is also a COFAA-IPN and an EDI-IPN fellow.

Author information

Author notes

  1. Horacio Lozano-Cobo

    Present address: Departamento de Hidrobiología, Universidad Autónoma Metropolitana, Unidad Iztapalapa. Av. San Rafael Atlixco No. 186, Col. Vicentina, 09340, Mexico, Mexico

Authors and Affiliations

  1. Departamento de Plancton y Ecología Marina, Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, Av. IPN s/n, 23096, La Paz, B.C.S, Mexico

    Horacio Lozano-Cobo & Jaime Gómez-Gutiérrez

  2. Laboratorio de Parasitología, Departamento Académico de Ciencias Marinas y Costeras, Universidad Autónoma de Baja California Sur, km 5.5 Carretera al Sur, 23080, La Paz, B.C.S, Mexico

    María del Carmen Gómez del Prado-Rosas

  3. Departamento Académico de Ingeniería en Pesquerías, Universidad Autónoma de Baja California Sur, Km 5.5 Carretera al Sur, 23080, La Paz, B.C.S, Mexico

    Claudia A. Silva-Segundo

  4. Laboratorio de Helmintología, Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Tercer circuito s/n, Ciudad Universitaria, 04510, Mexico, Mexico

    Alejandro Oceguera-Figueroa

Authors
  1. Horacio Lozano-Cobo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María del Carmen Gómez del Prado-Rosas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Claudia A. Silva-Segundo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alejandro Oceguera-Figueroa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jaime Gómez-Gutiérrez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jaime Gómez-Gutiérrez.

Ethics declarations

Conflict of Interest

The authors declare that they have not conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (TIFF 1097 KB)

Supplementary file2 (DOCX 1152 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lozano-Cobo, H., Gómez del Prado-Rosas, M.d.C., Silva-Segundo, C.A. et al. Molecular Identification of Plerocercoids of Clistobothrium montaukensis (Cestoda: Phyllobothriidea) Parasitizing the King of Herrings Regalecus glesne. Acta Parasit. 66, 1586–1592 (2021). https://doi.org/10.1007/s11686-021-00400-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11686-021-00400-9

Keywords

Search

Navigation