Abstract
Kudoid myxozoans have been reported causing serious chronic problems in marine fisheries, by reducing the market value of infected fish through pathological damage to the host musculature. We report here the overall prevalence of a Kudoa species in 84/277 (30.3%) fishes from 20 different species of high commercial value captured between October 2011 and December 2013 from the United Nations Food and Agriculture Organization (FAO) 34 commercial fishing area, near the coast of the Canary Islands (Spain). Macroscopic examination showed myxozoan-like cysts in skeletal muscle from 5 of the 20 fish species examined, with the following prevalences: Pagellus acarne (86.7%), Pagellus erythrinus (46.5%), Serranus cabrilla (27.8%), Spondyliosoma cantharus (19.4%), and Sarpa salpa (28.6%). Infection intensity was determined based on spore counts following muscle tissue digestion. Morphometric studies to characterize the species and DNA sequence analysis results suggest that these infections are attributable to a Kudoa species closely related to Kudoa trachuri. This paper reports the first study on a multivalvulidan species to be identified from the Canary Islands. Furthermore, this is the first report of Kudoa parasites in all of the hosts mentioned above, with the exception of P. acarne.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abe N, Maehara T (2013) Molecular characterization of kudoid parasites (Myxozoa: Multivalvulida) from somatic muscles of Pacific bluefin (Thunnus orientalis) and yellowfin (T. albacores) tuna. Acta Parasitol 58:226–230. https://doi.org/10.2478/s11686-013-0130-1
Adlard RD, Bryant MS, Whipps CM, Kent ML (2005) Multivalvulid myxozoans from eastern Australia: three new species of Kudoa from scombrid and labrid fishes of the Great Barrier Reef, Queensland, Australia. J Parasitol 91:1138–1142. https://doi.org/10.1645/GE-368R.1
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC146917/pdf/253389.pdf
Blaylock RB, Bullard SA, Whipps CM (2004) Kudoa hypoepicardialis n. sp.(Myxozoa: Kudoidae) and associated lesions from the heart of seven perciform fishes in the northern Gulf of Mexico. J Parasitol 90:584–593. https://doi.org/10.1645/GE-161R
Burger MAA, Adlard RD (2010) Four new species of Kudoa Meglitsch, 1947 (Myxosporea: Multivalvulida) from Australia with recommendations for species descriptions in the Kudoidae. Parasitology 137:793–814. https://doi.org/10.1017/S0031182009991557
Burger MAA, Adlard RD (2011) Low host specificity in the Kudoidae (Myxosporea: Multivalvulida) including 17 new host records for Kudoa thalassomi. Folia Parasitol 58:1–16 https://pdfs.semanticscholar.org/945d/da68d3c775ce2392edd722d871359806cb4b.pdf
Burger MAA, Barnes AC, Adlard RD (2008) Wildlife as reservoirs for parasites infecting commercial species: host specificity and a redescription of Kudoa amamiensis from teleost fish in Australia. J Fish Dis 31:835–844. https://doi.org/10.1111/j.1365-2761.2008.00958.x
Eiras JC, Saraiva A, Cruz C (2014) Synopsis of the species of Kudoa Meglitsch, 1947 (Myxozoa: Myxosporea: Multivalvulida). Syst Parasitol 87:153–180. https://doi.org/10.1007/s11230-013-9461-4
FAO 1990-2018. FAO Major Fishing Areas. Atlantic, Eastern Central (Major Fishing Area 34). CWP Data Collection. In: FAO Fisheries and Aquaculture Department [online]. Rome. Updated 1 October 2004. [cited 25 January 2018]
Fregel R, González A, Cabrera VM (2010) Improved ethanol precipitation of DNA. Electrophoresis 31:1–3. https://doi.org/10.1002/elps.200900721
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98 http://brownlab.mbio.ncsu.edu/JWB/papers/1999Hall1.pdf
Heiniger H, Adlard RD (2012) Host specificity and local infection dynamics of Kudoa leptacanthae n. sp (Multivalvulida: Kudoidae) from the pericardial cavity of two Zoramia spp. (Perciformes: Apogonidae) at Lizard Island lagoon, Queensland, Australia. Parasitol Int 61:697–706. https://doi.org/10.1016/j.parint.2012.08.001
Heiniger H, Cribb TH, Adlard RD (2013) Intra-specific variation of Kudoa spp. (Myxosporea: Multivalvulida) from apogonid fishes (Perciformes), including the description of two new species, K. cheilodipteri n. sp. and K. cookii n. sp., from Australian waters. Syst Parasitol 84:193–215. https://doi.org/10.1007/s11230-012-9400-9
Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453
Iwashita Y, Kamijo Y, Nakahashi S, Shindo A, Yokoyama K, Yamamoto A, Omori Y, Ishikura K, Fujioka M, Hatada T, Takeda T, Maruyama K, Imai H (2013) Food poisoning associated with Kudoa septempunctata. J Emerg Med 44:943–945. https://doi.org/10.1016/j.jemermed.2012.11.026
Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156. https://doi.org/10.1111/j.1365-2761.1989.tb00287.x
Mansour L, Harrath AH, Abd-Elkader OH, Alwasel S, Abdel-Baki AA, Al Omar SY (2014) Structural and molecular characterization of Kudoa quraishii n. sp. from the trunk muscle of the Indian mackerel Rastrelliger kanagurta (Perciforme, Scombridae) in Saudi Arabia coasts. Parasitol Res 113:1361–1370. https://doi.org/10.1007/s00436-014-3775-2
Marshall WL, Sitja-Bobadilla A, Brown HM, Macwilliam T, Richmond Z, Lamson H, Morrison DB, Afonso LO (2016) Long-term epidemiological survey of Kudoa thyrsites (Myxozoa) in Atlantic salmon (Salmo salar L.) from commercial aquaculture farms. J Fish Dis 39:929–946. https://doi.org/10.1111/jfd.12429
Matsukane Y, Sato H, Tanaka S, Kamata Y, Sugita-Konishi Y (2011) Kudoa iwatai and two novel Kudoa spp., K. trachuri n. sp. and K. thunni n. sp.(Myxosporea: Multivalvulida), from daily consumed marine fish in western Japan. Parasitol Res 108:913–926. https://doi.org/10.1007/s00436-010-2133-2
PEACAN (2014). Plan Estratégico de la Acuicultura en Canarias (PEACAN) 2014-2020. Consejería de Agricultura, Ganadería, pesca y Aguas del Gobierno de Canarias. Unión Europea. Fondo Europeo de Pesca
Popescu I, Ortega Gras JJ (2013) Fisheries in the Canary Islands. Fisheries, European Parliament. Directorate-General FOR Internal Policies. Policy Department B: Structural and Cohesion Policies. EU publications. https://doi.org/10.2861/18051
Samaranayaka AGP, Ho TCW, Li-Chan ECY (2007) Correlation of Kudoa spore counts with proteolytic activity and texture of fish mince from Pacific hake (Merluccius productus). J Aquat Food Prod Technol 15:75–93. https://doi.org/10.1300/J030v15n04_06
Sato H, Kasai A (2016) Kudoa species (Myxozoa: Myxosporea: Multivalvulida) recorded in Japan or its surrounding natural waters (1930-2016). Jpn J Vet Parasitol 15:111–138
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
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
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
Tuya F, Boyra A, Sanchez-Jerez P, Haroun RJ (2005) Multivariate analysis of the bentho-demersal ichthyofauna along soft bottoms of the Eastern Atlantic: comparison between unvegetated substrates, seagrass meadows and sandy bottoms beneath sea-cage fish farms. Mar Biol 147:1229–1237. https://doi.org/10.1007/s00227-005-0018-1
Whipps CM, Kent ML (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Eukaryot Microbiol 53:364–373 https://dx.doi.org.bibproxy.ulpgc.es/10.1111/j.1550-7408.2006.00114.x
Whipps CM, Adlard RD, Bryant MS, Kent ML (2003) Two unusual myxozoans, Kudoa quadricornis n. sp. (Multivalvulida) from the muscle of goldspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp. (Multivalvulida) from the muscle of Spanish mackerel (Scomberomorus commerson) from the Great Barrier Reef, Australia. J Parasitol 89:168–173. https://doi.org/10.1645/0022-3395(2003)089[0168:TUMKQN]2.0.CO;2
Whipps CM, Grossel G, Adlard RD, Yokoyama H, Bryant MS, Munday BL, Kent ML (2004) Phylogeny of the Multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. J Parasitol 90:618–622. https://doi.org/10.1645/GE-153R
Acknowledgments
We would like to thank Dr. Emilio Soler Onís for his assistance and technical advise in taking optical microscopy photos. We are also grateful to anonymous reviewers for their valuable comments that improved the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Christopher Whipps
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rodríguez-Ponce, E., Betancor, E., Steinhagen, D. et al. Kudoa sp. (Myxozoa, Multivalvulida): first report in five commercial fish species from the Canary Islands-FAO 34 (Macaronesia-Spain). Parasitol Res 118, 2567–2574 (2019). https://doi.org/10.1007/s00436-019-06415-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06415-6