Diphyllobothrium sprakeri n. sp. (Cestoda: Diphyllobothriidae): a hidden broad tapeworm from sea lions off North and South America
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
Parazitologický ústav, Akademie Věd České Republiky
177603
Consejo Nacional de Ciencia y Tecnología
PubMed
33888151
PubMed Central
PMC8063393
DOI
10.1186/s13071-021-04661-1
PII: 10.1186/s13071-021-04661-1
Knihovny.cz E-zdroje
- Klíčová slova
- Helminths, Otaria flavescens, Otariidae, Parasites, Pinnipedia, Zalophus californianus, cox1, lsrDNA,
- MeSH
- difylobotriáza veterinární MeSH
- Diphyllobothrium anatomie a histologie klasifikace genetika izolace a purifikace MeSH
- fylogeneze MeSH
- lachtani parazitologie MeSH
- mitochondriální geny MeSH
- střeva parazitologie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Jižní Amerika MeSH
- Severní Amerika MeSH
BACKGROUND: The systematic of several marine diphyllobothriid tapeworms of pinnipeds has been revised in recent years. However, 20 species of Diphyllobothrium from phocids and otariids are still recognized as incertae sedis. We describe a new species of Diphyllobothrium from the intestine of California sea lions Zalophus californianus (Lesson) (type-host) and South American sea lions Otaria flavescens (Shaw). METHODS: Zalophus californianus from the Pacific coast of the USA and O. flavescens from Peru and Argentina were screened for parasites. Partial fragments of the large ribosomal subunit gene (lsrDNA) and the cytochrome c oxidase subunit 1 (cox1) mitochondrial gene were amplified for 22 isolates. Properly fixed material from California sea lions was examined using light and scanning electron microscopy. RESULTS: A total of four lsrDNA and 21 cox1 sequences were generated and aligned with published sequences of other diphyllobothriid taxa. Based on cox1 sequences, four diphyllobothriid tapeworms from O. flavescens in Peru were found to be conspecific with Adenocephalus pacificus Nybelin, 1931. The other newly generated sequences fall into a well-supported clade with sequences of a putative new species previously identified as Diphyllobothrium sp. 1. from Z. californianus and O. flavescens. A new species, Diphyllobothrium sprakeri n. sp., is proposed for tapeworms of this clade. CONCLUSIONS: Diphyllobothrium sprakeri n. sp. is the first diphyllobothriid species described from Z. californianus from the Pacific coast of North America, but O. flavescens from Argentina, Chile and Peru was confirmed as an additional host. The present study molecularly confirmed the first coinfection of two diphyllobothriid species in sea lions from the Southern Hemisphere.
1 I Schmalhausen Institute of Zoology NAS of Ukraine 15 Bogdan Khmelnytsky Street Kyiv 01030 Ukraine
Zobrazit více v PubMed
Caira JN, Jensen K. Planetary biodiversity inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. Lawrence: University of Kansas, Natural History Museum, Special Publication No. 25; 2017.
Hernández-Orts JS, Scholz T, Brabec J, Kuzmina T, Kuchta R. High morphological plasticity and global geographical distribution of the Pacific broad tapeworm Adenocephalus pacificus (syn. Diphyllobothrium pacificum): molecular and morphological survey. Acta Trop. 2015;149:168–178. doi: 10.1016/j.actatropica.2015.05.017. PubMed DOI
Kuchta R, Scholz T. Diphyllobothriidea. In: Caira JN, Jensen K, editors. Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. Lawrence: University of Kansas, Natural History Museum, Special Publication No. 25; 2017. p. 167–89.
Waeschenbach A, Brabec J, Scholz T, Littlewood DTJ, Kuchta R. The catholic taste of broad tapeworms—multiple routes to human infection. Int J Parasitol. 2017;47:831–843. doi: 10.1016/j.ijpara.2017.06.004. PubMed DOI
Hernández-Orts JS, Scholz T, Brabec J, Kuzmina T, Kuchta R. Does the number of genital organs matter? Case of the seal tapeworm Diphyllobothrium (syn. Diplogonoporus) tetrapterum (Cestoda: Diphyllobothriidea) Can J Zool. 2018;96:193–204. doi: 10.1139/cjz-2017-0013. DOI
Schaeffner BC, Ditrich O, Kuchta R. A century of taxonomic uncertainty: re-description of two species of tapeworms (Diphyllobothriidea) from Arctic seals. Polar Biol. 2018;41:2543–2559. doi: 10.1007/s00300-018-2396-0. DOI
Mariaux J, Kuchta R, Hoberg EP. 2017. Tetrabothriidea Baer, 1954. In: Caira JN, Jensen K, editors. Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. Lawrence: University of Kansas, Natural History Museum, Special Publication No. 25;2017: p. 357–70.
Scholz T, Kuchta R, Brabec J. Broad tapeworms (Diphyllobothriidae), parasites of wildlife and humans: recent progress and future challenges. Int J Parasitol Parasites Wildl. 2019;9:359–369. doi: 10.1016/j.ijppaw.2019.02.001. PubMed DOI PMC
Carretta JV, Forney KA, Lowry MS, Barlow J, Baker J, Hanson B, Muto MM. U.S. Pacific Marine Mammal Stock Assessments: 2007. Washington: US Department of Commerce NOAA Technical Memorandum, NMFS–SWFSC–414; 2007.
McClatchie S, Field J, Thompson AR, Gerrodette T, Lowry M, Fiedler PC, et al. Food limitation of sea lion pups and the decline of forage off central and southern California. R Soc Open Sci. 2016;3:150628. doi: 10.1098/rsos.150628. PubMed DOI PMC
Stunkard HW. Variation and criteria for generic and specific determination of diphyllobothriid cestodes. J Helminthol. 1965;39:281–296. doi: 10.1017/S0022149X0002068X. PubMed DOI
Dailey MD, Hill BL. A survey of metazoan parasites infesting the California (Zalophus californianus) and Steller (Eumetopias jubatus) sea lion. Bull South Calif Acad Sci. 1970;69:126–132.
Dailey MD, Brownell RL., Jr . A checklist of marine mammal parasites. In: Ridgway SH, editor. Mammals of the sea, biology and medicine. Springfield: Charles C. Thomas; 1972. pp. 528–589.
Margolis L, Dailey MD. Revised annotated list of parasites from sea mammals caught of the west coast of North America. NOAA technical report NMFS, SSRF-647. Seattle: National Oceanic and Atmospheric Administration; 1972.
Dailey MD. The distribution and intraspecific variation of helminth parasites in pinnipeds. Rapp P-V Réun Cons Int Explor Mer. 1975;169:338–352.
Dailey MD. Baseline data on parasites from marine mammals in the Southern California Bight area. Marine mammal and seabird survey of the Southern California Bight area. Vol. III. Principal investigator's reports. Book 1. Pinnipedia, Cetacea and Parasitology. Santa Cruz: California University; 1978. p. 442–72.
Felix JR. Reported incidences of parasitic infections in marine mammals from 1892 to 1978. Lincoln: Zea E-Books; 2013.
Kuzmina TA, Spraker TR, Kudlai O, Lisitsyna O, Zabludovskaja SO, Karbowiak G, et al. Metazoan parasites of California sea lions (Zalophus californianus): a new data and review. Int J Parasitol Parasites Wildl. 2018;7:326–334. doi: 10.1016/j.ijppaw.2018.09.001. PubMed DOI PMC
Crespo EA, Oliva D, Dans S, Sepúlveda M. Current status of the South American sea lion along the distribution range. Valparaíso: Editorial Universidad de Valparaíso; 2012.
Cárdenas-Alayza S, Crespo EA, Oliveira LR. Otaria byronia. The IUCN Red List of Threatened Species; 2016. 10.2305/IUCN.UK.2016-1.RLTS.T41665A61948292.en
Baylis HA, in (sic) Hamilton JE. The Southern sea lion, Otaria byronia (De Blainville). Discovery Rep. 1934;8:306.
Markowski S. The cestodes of seals from the Antarctic. Brit Bull Nat Hist. 1952;1:125–150.
Baer JG, Miranda H, Fernandez W, Medina TJ. Human diphyllobothriasis in Peru. Z Parasitenkd. 1967;28:227–289. doi: 10.1007/BF00260267. PubMed DOI
Hermosilla C, Hirzmann J, Silva LMR, Scheufen S, Prenger-Berninghoff E, Ewers C, et al. Gastrointestinal parasites and bacteria in free-living South American sea lions (Otaria flavescens) in Chilean Comau Fjord and new host record of a Diphyllobothrium scoticum-like cestode. Front Mar Sci. 2018;5:459. doi: 10.3389/fmars.2018.00459. DOI
Ebmer D, Navarrete MJ, Muñoz P, Flores LM, Gärtner U, Brabec J, et al. Anthropozoonotic parasites circulating in synanthropic and Pacific colonies of South American sea lions (Otaria flavescens): Non-invasive techniques data and a review of the literature. Front Mar Sci. 2020;7:543829. doi: 10.3389/fmars.2020.543829. DOI
Spraker TR. Basic Necropsy Procedures. In: McCurnin DM, editor. Clinical textbook for the animal health technician. London: W.B. Saunders Company; 1985. pp. 4702–4816.
Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, et al. Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phylogenet Evol. 2008;48:369–371. doi: 10.1016/j.ympev.2008.03.024. PubMed DOI
Littlewood DTJ, Curini-Galletti M, Herniou EA. The interrelationships of Proseriata (Platyhelminthes: Seriata) flatworms tested with molecules and morphology. Mol Phylogenet Evol. 2000;16:449–466. doi: 10.1006/mpev.2000.0802. PubMed DOI
Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda) Int J Parasitol. 2003;33:733–755. doi: 10.1016/S0020-7519(03)00049-3. PubMed DOI
Bowles J, McManus DP. Genetic characterization of the Asian Taenia, a newly described taeniid cestode of humans. Am J Trop Med Hyg. 1994;50:33–44. doi: 10.4269/ajtmh.1994.50.1.TM0500010033. PubMed DOI
Wicht B, Yanagida T, Scholz T, Ito A, Jiménez JA, Brabec J. Multiplex PCR for differential identification of broad tapeworms (Cestoda: Diphyllobothrium) infecting humans. J Clin Microbiol. 2010;48:3111–3116. doi: 10.1128/JCM.00445-10. PubMed DOI PMC
Brabec J, Scholz T, Králová-Hromadová I, Bazsalovicsová E, Olson PD. Substitution saturation and nuclear paralogs of commonly employed phylogenetic markers in the Caryophyllidea, an unusual group of non-segmented tapeworms (Platyhelminthes) Int J Parasitol. 2012;42:259–267. doi: 10.1016/j.ijpara.2012.01.005. PubMed DOI
Gomez-Puerta LA, Alarcon V, Pacheco J, Franco F, Lopez-Urbina MT, Gonzalez AE. Molecular and morphological evidence of Taenia omissa in pumas (Puma concolor) in the Peruvian Highlands. Rev Bras Parasitol Vet. 2016;25:368–373. doi: 10.1590/S1984-29612016046. PubMed DOI
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–2179. doi: 10.1093/nar/gkh340. PubMed DOI PMC
Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772. doi: 10.1038/nmeth.2109. PubMed DOI PMC
Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. PubMed DOI
Edler D, Klein J, Antonelli A, Silvestro D. raxmlGUI 2.0; 2019. https://antonellilab.github.io/raxmlGUI/
Rambaut A. FigTree v. 2.0; 2018. http://tree.bio.ed.ac.uk/software/
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC
Chervy L. Unified terminology for cestode microtriches: a proposal from the International Workshops on Cestode Systematics in 2002–2008. Folia Parasitol. 2009;56:199–230. doi: 10.14411/fp.2009.025. PubMed DOI
Delyamure SL, Skryabin AS, Serdiukov AM. Diphyllobothriata—Flatworm parasites of man, mammals and birds. In: Sudarikov VE, editor. Principles of Cestodology. Vol. 11. Moscow: Izdatel’stvo Nauka: 1985, p. 200. (in Russian)
Rennie J, Reid A. The Cestoda of the Scottish Antarctic Expedition (Scotia) Trans R Soc Edinburgh. 1912;48:441–453. doi: 10.1017/S0080456800002945. DOI
Fuhrmann O. Die Cestoden der Deutschen Südpolar-Expedition 1901–1903. Deutsche Südpol-Exped. 1920;1901–1903(16):469–524.
Johnston TH. The Cestoda of the Australasian Antarctic Expedition. Sci Rep Aust Antarctic Exped. 1937;10:1–74.
Yurakhno MV, Maltsev VN. Diphyllobothrium lobodoni sp. n. (Cestoda: Diphyllobothriidae)—The parasite of the crabeater seal. Parazitologiya. 1994;28:270–5. (in Russian) PubMed
Wojciechowska A, Zdzitowiecki K. Cestodes of Antarctic seals. Acta Parasitol. 1995;40:125–131.
Szteren D, Aurioles D, Gerber LR. Population status and trends of the California sea lion (Zalophus californianus californianus) in the Gulf of California, Mexico. In: Trites AW, Atkinson SK, DeMaster DP, Fritz LW, Gelatt TS, Rea LD, Wynne KM, editors. Sea Lions of the World. Fairbanks: Alaska Sea Grant College Program; 2006. pp. 369–384.
Yurakhno MV, Maltsev VN. An infection of seals from Antarctica with cestodes. Parazitologiya. 1997;31:81–89.
Kuzmina TA, Hernández-Orts JS, Lyons ET, Spraker TR, Kornyushyn VV, Kuchta R. The cestode community in northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska. Int J Parasitol Parasites Wildl. 2015;4:256–263. doi: 10.1016/j.ijppaw.2015.04.007. PubMed DOI PMC
Kuzmina TA, Kuzmin YI, Dzeverin I, Lisitsyna OI, Spraker TR, Korol EM, Kuchta R. Review of metazoan parasites of the northern fur seal (Callorhinus ursinus) and the analysis of the gastrointestinal helminth community of the population on St. Paul Island, Alaska. Parasitol Res. 2021;120:117–132. doi: 10.1007/s00436-020-06935-6. PubMed DOI
Mondragón Martínez AM. Identificación molecular de los estadios de plerocercoide y adulto de Diphyllobothrium sp. obtenidos de humanos, lobos marinos y peces. Bachelor Thesis. Lima: Universidad Ricardo Palma; 2017. p. 82. http://repositorio.urp.edu.pe/handle/urp/1007.
Kuchta R, Serrano-Martínez ME, Scholz T. Pacific broad tapeworm Adenocephalus pacificus as a causative agent of globally reemerging diphyllobothriosis. Emerg Infect Dis. 2015;21:1697–1703. doi: 10.3201/eid2110.150516. PubMed DOI PMC
Scholz T, Garcia HH, Kuchta R, Wicht B. Update on the human broad tapeworm (genus Diphyllobothrium), including clinical relevance. Clin Microbiol Rev. 2009;22:146–160. doi: 10.1128/CMR.00033-08. PubMed DOI PMC