Skip to main content
Log in

Diclidophora luscae (Monogenea: Diclidophoridae) in pouting, Trisopterus luscus (Linnaeus, 1758) from the northeast Atlantic; epidemiology, morphology, molecular and phylogenetic analysis

  • Fish Parasitology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Diclidophora (Monogenea) species are gill parasites with a stenoxenic specificity occurring only in Gadiformes. Epidemiological, morphological, molecular and phylogenetic studies were performed on 594 Diclidophora specimens collected from 213 Trisopterus luscus captured in the northeast Atlantic off the Portuguese coast during 2012, 2013 and 2020. Prevalence, parasite abundance and infection intensity were determined. Positive correlation between fish weight and length and infection intensity was observed. The effects of preservation on the parasite morphological features were studied, highlighting that specimen’s identification should be reinforced by molecular studies. A sequence of D. luscae capelanii from T. capelanus captured in the Mediterranean Sea included in the 28S rDNA molecular analysis was nested within a robust D. luscae clade. Data analysis suggested that this species is in fact D. luscae, which is compatible with T. luscus and T. capelanus. The identity of fish hosts was confirmed by barcoding. For the first time, data on the infection parameters is shown, highlighting the importance of including this parasite in the monitoring plans for a holistic approach with possible effects for the management of pouting resources aiming of attaining sustainable development and biodiversity conservation measures, according to the 14th objective of the 2030 agenda.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Armani A, Castigliego L, Tinacci L, Gianfaldoni D, Guidi A (2012) Multiplex conventional and real-time PCR for fish species identification of Bianchetto (juvenile form of Sardina pilchardus), Rossetto (Aphia minuta), and Icefish in fresh, marinated, and cooked products. Food Chem 133(1):184–192

    Article  CAS  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM et al (1997) Parasitology meets ecology on its own terms: Margolis et al revisited. J Parasitol 83:575–583

    Article  CAS  Google Scholar 

  • Calo-Mata P, Sotelo CG, Pérez-Martín RI et al (2003) Identification of gadoid fish species using DNA-based techniques. Eur Food Res Technol 217(3):259–264

    Article  CAS  Google Scholar 

  • Carneiro M, Martins R, Landi M et al (2014) Updated checklist of marine fishes (Chordata: Craniata) from Portugal and the proposed extension of the Portuguese continental shelf. Eur J Taxon 73:1–73

    Google Scholar 

  • Carneiro M, Martins R, Reiner F et al (2019) Ichthyofauna of Portugal: taxonomic diversity, common and scientific names of marine fishes. Instituto Português do Mar e da Atmosfera, I.P, Vol I:144

  • Carr SM, Kivlichan DS, Pepin P et al (1999) Molecular systematics of gadid fishes implications for the biogeographic origin of Pacific species. Can J Zool 7:19–26

    Article  Google Scholar 

  • Dawes B (1947) The trematoda of British fishes. The Ray Society, London

    Book  Google Scholar 

  • Delling B, Noren M, Kullander SO et al (2011) Taxonomic review of the genus Trisopterus (Teleostei: Gadidae) with recognition of the capelin Trisopterus capelanus as a valid species. J Fish Biol 79:1236–1260

    Article  CAS  Google Scholar 

  • Felício M, Gonçalves M, Machado I et al (2021) Spatial patterns of demersal communities from bottom trawl on the Portuguese North Coast (continental shelf). Reg Stud Mar Sci 44:101769

    Google Scholar 

  • Froese R, Pauly D Editors (2021) FishBase. World Wide Web electronic publication. www.fishbase.org, version (06/2021). Accessed 21 Oct 2021

  • Gonzalez EG, Cunha RL, Sevilla RG et al (2012) Evolutionary history of the genus Trisopterus. Mol Phylogenet Evol 62(3):1013–1018

    Article  CAS  Google Scholar 

  • Halton DW (1979) The surface topography of a monogenean Diclidophora merlangi revealed by scanning electron microscopy. Z Parasitenkd 61:1–12

    Article  CAS  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  Google Scholar 

  • Hassouna N, Mithot B, Bachellerie JP (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(8):3563–3583

    Article  CAS  Google Scholar 

  • Johansen S, Johansen T (1994) Sequence analysis of 12 structural genes and a novel non-coding region from mitochondrial DNA of Atlantic cod, Gadus Morhua. Biochim Biophys Acta 1218(2):213–217

    Article  CAS  Google Scholar 

  • Jovelin R, Justine JL (2001) Phylogenetic relationships within the polyopisthocotylean monogeneans (Platyhelminthes) inferred from partial 28S rDNA sequences. Int J Parasitol 31(4):393–401

    Article  CAS  Google Scholar 

  • Kearn GC, Vasconcelos ME (1979) Preliminary list of monogenean parasites of Portuguese marine fishes, with a note on Enoplocotyle minima Tagliani, 1912. Bol Inst Nac Inv 1:25–34

  • Kumar S, Stecher G, Li M et al (2018) MEGA X: Molecular evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  Google Scholar 

  • Landa J, Cañás L (2017) Spraguea lophii (Microsporidia) parasitizing blackbellied angler (Lophius budegassa) and angler (L. piscatorius) in European Atlantic waters. J Sea Res 130:210–216

    Article  Google Scholar 

  • Lester RJG (2012) Overdispersion in marine parasites. J Parasitol 98:718–721

  • Lester RJG, McVinish R (2016) Does moving up a food chain increase aggregation in parasites? J R Soc Interface 13:20160102

  • Llewellyn J (1958) The adhesive mechanisms of monogenetic trematodes: the attachment of species of the Diclophoridae to the gills of gadoid fishes. J Mar Biol Assoc UK 37:67–79

    Article  Google Scholar 

  • Llewellyn J, MacDonald S, Green JE (1980) Host-specificity and speciation in Diclidophoran (monogenean) gill parasites of Trisopteran (Gadoid) Fishes at Plymouth. J Mar Biol Assoc UK 60:73–79

    Article  Google Scholar 

  • MacKenzie K, Abaunza P (2014) Parasites as biological tags. In: Cadrin SX, Friedland KD, Waldman JR.(eds) Stock Identification Methods, 1st edn. Elsevier, Academic Press, pp 211–226

  • MacKenzie K, Campbell N, Mattiucci S et al (2008) Parasites as biological tags for stock identification of Atlantic horse mackerel, Trachurus trachurus L. Fish Res 89:136–145

    Article  Google Scholar 

  • Marcogliese DJ (2008) The impact of climate change on the parasites and infectious diseases of aquatic animals. Rev Sci Off Int Epiz 27:467–484

    Article  CAS  Google Scholar 

  • Marôco J (2018) Análise Estatística com o SPSS Statistics. 8th edn. ReportNumber, Lisbon

  • Mendoza-Franco E, Tun MCR, Anchevida AJD et al (2018) Morphological and molecular (28SrRNA) data of monogeneans (Platyhelminthes) infecting the gill lamellae of marine fish in the Campeche Bank, southest Gulf of Mexico. Zookys 783:125–161

    Article  Google Scholar 

  • Moller PR, Jordan AD, Graulund P et al (2002) Phylogenetic position of the cryopelagic codfish genus Arctogadus drjagin 1932 based on partial mitochondrial cytochrome b sequences. Polar Biol 25(5):342–349

    Article  Google Scholar 

  • Morsy K, Shazly M, Abdel-Gawad M et al (2018) The first report of two monogenean gill parasites assigned to Diclidophora merlangi (Diclidophoridae) and Loxuroides pricei (Axinidae) from brushtooth lizardfish and red porgy seabream of the Red Sea, Egypt. Vet Res Forum 9:163–169

    PubMed  PubMed Central  Google Scholar 

  • Oliva ME, Sepulveda FA, Gonzalez MT (2014) Parapedocotyle prolatili gen. n. et sp. n., a representative of a new subfamily of the Diclidophoridae (Monogenea), a gill parasite of Prolatilus jugularis (Teleostei: Pinguipedidae) from Chile. J Folia Parasitol 61(6):543–548

    Article  CAS  Google Scholar 

  • Palm HW (2011) Fish parasites as biological indicators in a changing world: can we monitor environmental impact and climate change? In: Mehlhorn H (ed) Progress in Parasitology. Parasitology Research Monographs 2:223–250

  • Perdiguero-Alonso D, Montero FM, Raga JÁ et al (2006) Diclidophora merlangi (Monogenea: Diclidophoridae) on Atlantic cod, Gadus Morhua. J Parasitol 92(4):697–702

    Article  Google Scholar 

  • Quiazon KMA (2015) Updates on aquatic parasites in fisheries: implications to food safety, food security and environmental protection. J Coast Zone Manag 18:1–7

    Article  Google Scholar 

  • Ramos P (2012) Anisakis e Anisaquiose. Riscos e Alimentos 4:30–33

    Google Scholar 

  • Ramos P, Grade A, Sousa A et al (2013) Report about Diclidophora luscae infecting pouting, Trisopterus luscus from the Northeast Atlantic of the Portuguese coast based on morphological and ultrastructural studies. Livro de Resúmenes, XVIII SOCEPA Congress and International Meeting of Parasitologists from Spain, France, Italy and Portugal. 17th to 20th September, Las Palmas, Gran Canaria, 170

  • Ramos P, Grade A, Sousa A et al (2014a) Fanecas do Atlântico Nordeste da Costa Portuguesa Infectadas com Diclidophora luscae. Estudos Epidemiológico, Morfológico e Ultra estrutural – Dados Recentes. Congresso da Sociedade Portuguesa de Ciências Veterinárias. Livro de Resumos Ciências Veterinárias: Praxis e Futuro. 3rd to 5th April, INIAV, Oeiras, p 112

  • Ramos P, Rosa F, Oliveira MM et al (2014b) Morphological and ultrastructural characterization of Diclidophora luscae and comparison of the metric variables in different methodologies applied to species characterization. Proceedings of the XXXTH Congress of the European Association of Veterinary Anatomists. Cluj-Napoca, Romania, July 23 – 26. Anat Histol Embryol 43(Supply. 1):75–76

    Google Scholar 

  • Ramos P, Carvalho R, Rosa F et al (2019) Huffmanela lusitana sp. n. (Nematoda: Trichosomoididae) infecting pouting, Trisopterus luscus (Teleostei: Gadidae) off the Atlantic coast of Portugal. Int J Parasitol Parasites Wildl 9:266–273

    Article  Google Scholar 

  • Reiczigel J, Marozzi M, Fábián I, Rózsa L (2019) Biostatistics for Parasitologists - A Primer to Quantitative Parasitology. Trends Parasitol 35(4):277–281

    Article  Google Scholar 

  • Rubec LA, Dronen NO (1994) Revision of the genus Diclidophora KrØyer, 1838 (Monogenea: Diclidophoridae), with the proposal of Macrouridophora n. g. Syst Parasitol 28:159–185

    Article  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Strona G, Stefani F, Galli P (2010) Monogenoidean parasites of Italian marine fish: an updated checklist. Ital J Zool 77(4):419–437

    Article  Google Scholar 

  • Teixeira CM, Gamito R, Leitão F et al (2014) Trends in landings of fish species potentially affected by climate change in Portuguese fisheries. Reg Environ Change 14:657–669

    Article  Google Scholar 

  • Teletchea F, Laudet V, Hanni C (2006) Phylogeny of the Gadidae (sensu Svetovidov, 1948) based on their morphology and two mitochondrial genes. Mol Phylogenet Evol 38(1):189–199

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Marta Gonçalves, to their assistance to obtain the third sample. The authors are grateful to Kenneth MacKenzie for his kind comments and review of the manuscript.

Funding

This research was funded by SANAQUA MAR-02.05.01-FEAMP-0004 and PREVINE PTDC/ASP-PES/29576/2017 projects through national funds. Thanks also are due to FCT/MCTES for the financial support to CESAM (UIDP/50017/2020 + UIDB/50017/2020 + LA/P/0094/2020) and to CIIMAR (UID/QUI/50006/2019, UIDB/50006/2020, UIDP/50006/2020, UIDB/04423/2020 and UIDP/04423/2020), through national funds, and to Project ReNATURE –Valorization of the Natural Endogenous Resources of the Centro Region (Centro2020, Centro-01–0145-FEDER-000007). Raquel Varandas was funded by FCT (SFRH/BD/130172/2017).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paula Ramos.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Matthew Thomas Wayland

Publisher's note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramos, P., Varandas, R., Conceição, I.L. et al. Diclidophora luscae (Monogenea: Diclidophoridae) in pouting, Trisopterus luscus (Linnaeus, 1758) from the northeast Atlantic; epidemiology, morphology, molecular and phylogenetic analysis. Parasitol Res 121, 2517–2535 (2022). https://doi.org/10.1007/s00436-022-07591-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-022-07591-8

Keywords

Navigation