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Helminth communities of endemic cyprinoids of the Apennine Peninsula, with remarks on ectoparasitic monogeneans, and a description of four new Dactylogyrus Diesing, 1850 species

. 2021 Jul ; 148 (8) : 1003-1018. [epub] 20210412

Language English Country England, Great Britain Media print-electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

The fauna of the Apennine Peninsula is, in comparison to other southern European peninsulas, relatively species-poor regarding the number of endemic cyprinoid species. Nonetheless, the recent introduction of non-native species has significantly increased the total number of freshwater species in this region. Such invasive species may represent a threat to the native fauna, associated among other things with the introduction of non-native parasites with their original hosts.In the present study, we investigated endemic cyprinoid species for the presence of helminth parasites. A total of 36 ectoparasitic monogenean species and five endoparasitic helminth species were collected from ten cyprinoid species in five localities in northern Italy. Out of 20 Dactylogyrus species (gill monogeneans specific to cyprinoids), four were identified as new to science and herein described: Dactylogyrus opertus n. sp. and Dactylogyrus sagittarius n. sp. from Telestes muticellus, Dactylogyrus conchatus n. sp. from T. muticellus and Protochondrostoma genei, and Dactylogyrus globulatus n. sp. from Chondrostoma soetta. All new Dactylogyrus species appear to be endemic to the Apennine Peninsula; however, they share a common evolutionary history with the endemic Dactylogyrus parasitizing cyprinoids of the Balkans. This common origin of cyprinoid-specific parasites supports a historical connection between these two (currently separated) geographical regions.

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Angelescu N (1974) Contributions to the knowledge of the parasitofauna of Danube fishes from the reservoir of Iron Gates. Travaux du Museum d'Histoire Naturelle ‘Grigore Antipa 15, 13–22.

Bakke TA, Cable J and Harris PD (2007) The biology of gyrodactylid monogeneans: the ‘Russian-doll killers’. Advances in Parasitology 64, 161–376. PubMed

Benovics M, Kičinjaová ML and Šimková A (2017) The phylogenetic position of the enigmatic Balkan Aulopyge huegelii (Teleostei: Cyprinidae) from the perspective of host-specific Dactylogyrus parasites (Monogenea), with a description of Dactylogyrus omenti n. sp. Parasites & Vectors 10, 547. PubMed PMC

Benovics M, Desdevises Y, Vukić J, Šanda R and Šimková A (2018) The phylogenetic relationships and species richness of host-specific Dactylogyrus parasites shaped by the biogeography of Balkan cyprinids. Scientific Reports 8, 13006. PubMed PMC

Benovics M, Desdevises Y, Šanda R, Vukić J and Šimková A (2020) Cophylogenetic relationships between Dactylogyrus (Monogenea) ectoparasites and endemic cyprinoids of the north-eastern European peri-Mediterranean region. Journal of Zoological Systematics and Evolutionary Research 58, 1–21.

Benovics M, Koubková B, Civáňová K, Rahmouni I, Čermáková K and Šimková A (2021) Diversity and phylogeny of Paradiplozoon species (Monogenea: Diplozoidae) parasitising endemic cyprinoids in the peri-Mediterranean area, with a description of three new Paradiplozoon species. Parasitology Research 120, 481–496. PubMed

Berkhout BW, Borregaard MK, Brandl R, Brändle M, Dehling DM, Hof C, Poulin R and Thieltges DW (2020) Host assemblages and environment shape β-diversity of freshwater parasites across diverse taxa at a continental scale. Global Ecology and Biogeography 29, 38–49.

Bianco PG (1990) Potential role of the paleohistory of the Mediterranean and Parathethys basins on the early dispersal of Euro-Mediterranean freshwater fishes. Ichthyological Exploration of Freshwaters 1, 167–184.

Bianco PG (1995) Mediterranean endemic freshwater fishes of Italy. Biological Conservation 72, 159–170.

Blažek R, Jarkovský J, Koubková B and Gelnar M (2008) Seasonal variation in parasite occurrence and microhabitat distribution of monogenean parasites of gudgeon Gobio gobio (L.). Helminthologia 45, 185–191.

Bona F, Buriola E, Cerioni S, Orecchia P and Paggi L (1995) Digenea. In Minelli A, Ruffo S and La Posta S (eds), Checklist Delle Specie Della Fauna Italiana, Fascicolo 5. Bologna, Italy: Edizioni Calderini, pp. 31 pp.

Buj I, Marčić Z, Ćaleta M, Šanda R, Geiger MF, Freyhof J, Machordom A and Vukić J (2017) Ancient connections among the European rivers and watersheds revealed from the evolutionary history of the genus Telestes (Actinopterygii; Cypriniformes). PLoS ONE 12, e0187366. PubMed PMC

Bush AO, Lafferty KD, Lotzs JM and Shostakll AW (1997) Parasitology meets ecology on its own terms: Margolis, et al. revisited. Journal of Parasitology 83, 575–583. PubMed

Chunchukova M and Kirin D (2018) New data on endohelminth communities of barbel Barbus barbus from the Bulgarian part of the River Danube. Helminthologia 55, 222–229. PubMed PMC

Clark NJ, Clegg SM, Sam K, Goulding W, Koane B and Wells K (2018) Climate, host phylogeny and the connectivity of host communities govern regional parasite assembly. Diversity and Distributions 24, 13–23.

Djikanovic V, Paunovic M, Nikolic V, Simonovic P and Cakic P (2012) Parasitofauna of freshwater fishes in the Serbian open waters: a checklist of parasites of freshwater fishes in Serbian open waters. Reviews in Fish Biology and Fisheries 22, 297–324.

Dubinina MN (1987) Class tapeworms-Cestoda Rudolphi, 1808. In Bauer ON (ed.), Key to the Parasites of Freshwater Fishes of the USSR. Leningrad, Russia: Nauka, Vol. 3, pp. 5–76, (in Russian).

Ergens R (1969) The suitability of ammonium picrate-glycerin in preparing slides of lower Monogenoidea. Folia Parasitologica 16, 320.

Ergens R and Lom J (1970) Causative Agents of Fish Diseases. Prague, Czech Republic: Academia, 384 pp.

Galaktionov K and Bustnes J (1999) Distribution patterns of marine bird digenean larvae in periwinkles along the southern coast of the Barents Sea. Diseases of Aquatic Organisms 37, 221–230. PubMed

Galli P, Stefani F, Zaccara S and Crosa G (2002) Occurrence of Monogenea in Italian freshwater fish (Po river basin). Parassitologia 44, 189–197. PubMed

Galli P, Stefani F, Benzoni F and Zullini A (2005) Introduction of alien host–parasite complexes in a natural environment and the symbiota concept. Hydrobiologia 548, 293–299.

Galli P, Strona G, Benzoni F, Crosa G and Stefani F (2007) Monogenoids from freshwater fish in Italy, with comments on aliens species. Comparative Parasitology 74, 264–272.

Georgiev B, Biserkov V and Genov T (1986) In toto staining method for cestodes with iron acetocarmine. Helminthologia 23, 279–281.

Gherardi F, Bertolino S, Bodon M, Casellato S, Cianfanelli S, Ferraguti M, Lori E, Mura G, Nocita A, Riccardi N, Rossetti G, Rota E, Scalera R, Zerunian S and Tricarico E (2008) Animal xenodiversity in Italian inland waters: distribution, modes of arrival, and pathways. Biological Invasions 10, 435–454.

Gibson DI, Jones A and Bray RA (2002) Keys to the Trematoda, Volume I. Wallingford, UK: CABI Publishing, 544 pp.

Gregory RD (1990) Parasites and host geographic range as illustrated by waterfowl. Functional Ecology 4, 645–654.

Gutiérrez-Galindo JF and Lacasa-Millán MI (2001) Study of the Monogenea of Cyprinidae in the Llobregat River, Notheastern Spain. II. Species composition on Barbus graellsii Steindachner, 1866. Revista Ibérica de Parasitologia 61, 91–96.

Harris PD, Shinn AP, Cable J and Bakke TA (2004) Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Systematic Parasitology 59, 1–27. PubMed

Hassouna N, Michot B and 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 Research 12, 3563–3583. PubMed PMC

Havlátová L, Ondračková M and Přikrylová I (2015) Monogenean parasites of Lepomis gibbosus Linnaeus introduced into the River Durance, France. Helminthologia 52, 323–330.

Hechinger RF and Lafferty KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proceedings of the Royal Society B: Biological Sciences 272, 1059–1066. PubMed PMC

Hussain HA, Mhaisen FT and Al-Rubaie AL (2007) Ectoparasitic infection of the common carp and silver carp fingerlings stocked during winter in Al-Shark Al-Awsat fish farm, Babylon province. Journal of University of Babylon for Pure and Applied Sciences 14, 204–219, (In Arabic with English summary).

International Commission on Zoological Nomenclature (2012) Amendment of articles 8, 9, 10, 21 and 78 of the international code of zoological nomenclature to expand and refine methods of publication. Bulletin of Zoological Nomenclature 69, 161–169. PubMed PMC

Jalali B and Barzegar M (2005) Dactylogyrids (Dactylogyridae: Monogenea) on common carp (Cyprinus carpio L.) in freshwaters of Iran and description of pathogenicity of D. sahuensis. Journal of Agricultural Science and Technology 7, 9–16.

Jansen PA and Bakke TA (1991) Temperature-dependent reproduction and survival of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes: Monogenea) on Atlantic salmon (Salmo salar L.). Parasitology 102, 105–112. PubMed

Joyeux CH and Baer JG (1936) Cestodes. Faune de France. vol. 30, Paris, France: Paul Lechevalier, 608 pp.

Kakacheva-Avramova D (1973) Helminth faunas in fish in rivers of the central and eastern Balkan mountains. Izvestiya na Tsentralnata Khelmintologichna Laboratoriya 16, 87–110.

Kamiya T, O'Dwyer K, Nakagawa S and Poulin R (2014) Host diversity drives parasite diversity: meta-analytical insights into patterns and causal mechanisms. Ecography 37, 689–697.

Katoh K, Misawa K, Kuma K and Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066. PubMed PMC

Kmentová N, Van Steenberge M, van den Audenaerde DFET, Nhiwatiwa T, Bukinga FM, N'sibula TM, Mulungula PM, Gelnar M and Vanhove MPM (2019) Co-introduction success of monogeneans infecting fisheries target Limnothrissa miodon differs between two non-native areas: the potential of parasites as a tag for introduction pathway. Biological Invasions 21, 757–773.

Koskivaara M, Valtonen ET and Prost M (1991) Seasonal occurrence of gyrodactylid monogeneans on the roach (Rutilus rutilus) and variations between four lakes of differing water quality in Finland. Aqua Fennica 21, 47–55.

Kottelat M and Freyhof J (2007) Handbook of European Freshwater Fishes. Berlin, Germany: Kottelat, Cornol and Freyhof, 646 pp.

Krasnov BR, Shenbrot GI, Khokhlova IS and Degen AA (2004) Relationship between host diversity and parasite diversity: flea assemblages on small mammals. Journal of Biogeography 31, 1857–1866.

Kuchta R, Scholz T and Bray RA (2008) Revision of the order Bothriocephalidea Kuchta, Scholz, Brabec & Bray, 2008 (Eucestoda) with amended generic diagnoses and keys to families and genera. Systematic Parasitology 71, 81–136. PubMed

Laimgruber S, Schludermann C, Konecny R and Chovanec A (2005) Helminth communities of the barbel Barbus barbus from large river systems in Austria. Journal of Helminthology 79, 143–149. PubMed

Landsberg JH, Blakesley BA, Reese RO, McRae G and Forstchen PR (1998) Parasites of fish as indicators of environmental stress. Environmental Monitoring and Assessment 51, 211–232.

Ling F, Tu X, Huang A and Wang G (2016) Morphometric and molecular characterization of Dactylogyrus vastator and D. intermedius in goldfish (Carassius auratus). Parasitological Research 115, 1755–1765. PubMed

Lühe M (1910) Parasitische Plattwürmer vol. II: Cestodes. Jena, Germany: Verlag von Gustav Fischer, 153 pp.

Lymbery AJ, Morine M, Kanani HG, Beatty SJ and Morgan DL (2014) Co-invaders: the effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife 3, 171–177. PubMed PMC

Maestri R, Shenbrot GI and Krasnov BR (2017) Parasite beta diversity, host beta diversity and environment: application of two approaches to reveal patterns of flea species turnover in Mongolia. Journal of Biogeography 44, 1880–1890.

Malmberg G (1957) Om forekomsten av Gyrodactylus pa svenska fiskar. Skrifter Utgivna av Sodra Sveriges Fiskeriforening. Arsskift 1956, 19–76.

Marchetto F, Zaccara S and Muenzel FM (2010) Phylogeography of the Italian vairone (Telestes muticellus, Bonaparte 1837) inferred by microsatellite markers: evolutionary history of a freshwater fish species with a restricted and fragmented distribution. BMC Evolutionary Biology 10, 111. PubMed PMC

Marcogliese DJ (2001) Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 1331–1352.

Mizelle JD (1936) New species of trematodes from the gills of Illinois fishes. American Midland Naturalist 17, 785–806.

Molnár K (1964) Zwei neue Monogenetische egelarten. Acta Veterinaria Academiae Scientiarum Hungaricae 14, 247–252.

Molnár K and Ghittino P (1977) Alcuni vermi monogenoidea in pesci provenienti dal fiume Po e da piscicolture italiane. Rivista Italiana di Piscicoltura ed Ittiopatologia 12, 110–111.

Moravec F (2001) Checklist of Metazoan Parasites of Fishes of the Czech Republic and Slovak Republic, 1873–2000. Prague, Czech Republic: Academia, 168 pp.

Moravec F (2013) Parasitic Nematodes of Freshwater Fishes of Europe. Prague, Czech Republic: Academia, 604 pp.

Moravec F and Amin A (1978) Some helminth parasites, excluding Monogenea, from fishes of Afghanistan. Acta Scientiarum Naturalium Brno 12, 1–45.

Nieberding CM and Olivieri I (2007) Parasites: proxies from host genealogy and ecology? Trends in Ecology and Evolution 22, 156–165. PubMed

Nieberding CM, Morand S, Libois R and Michaux JR (2004) A parasite reveals cryptic phylogeographic history of its host. The Proceedings of Royal Society of London B 271, 2559–2568. PubMed PMC

Nocita A, Tricarico E and Bertolino S (2017) Fine-scale analysis of heavily invaded Italian freshwater fish assemblages. Integrative Zoology 12, 500–511. PubMed

Pielou EC (1979) Biogeography. New York, USA: Wiley, 351 pp.

Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, Sunberg P and Thollesson M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371. PubMed

Poulin R (2007) Evolutionary Ecology of Parasites 2nd Edn., New Jersey, USA: Princeton University Press, 342 pp.

Protasova EN (1977) Bothriocephalids – tapeworm helminths of fish. In Ryzhikov KM (ed.), Principles of Cestodology, Vol. 8. Moscow, Russia: Nauka, 298 pp.

Pugachev ON, Gerasev PI, Gussev AV, Ergens R and Khotenowsky I (2009) Guide to Monogenoidea of Freshwater Fish of Palearctic and Amur Regions. Milan, Italy: Ledizione-Ledi Publishing, 564 pp.

Rambaut A, Drummon AJ, Xie D, Baele G and Suchard MA (2018) Posterior summarization in Bayesian phylogenetic using Tracer 1.7. Systematic Biology 67, 901–904. PubMed PMC

Řehulková E, Benovics M and Šimková A (2020) Uncovering the diversity of monogeneans (Platyhelminthes) on endemic cypriniform fishes of the Balkan Peninsula: new species of Dactylogyrus and comments on their phylogeny and host-parasite associations in a biogeographic context. Parasite 27, 66. PubMed PMC

Robalo JI, Almada VC, Levy A and Doadrio I (2007) Re-examination and phylogeny of the genus Chondrostoma based on mitochondrial and nuclear data and the definition of 5 new genera. Molecular Phylogenetics and Evolution 42, 362–372. PubMed

Rohde K (1979) A critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. The American Naturalist 114, 648–671.

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA and Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across large model space. Systematic Biology 61, 539–542. PubMed PMC

Rózsa L, Reiczigel J and Majoros G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86, 228–232. PubMed

Scholz T (1989) Amphilinida and Cestoda, parasites of fish in Czechoslovakia. Acta Scientiarum Naturalium Brno 23, 1–56.

Scholz T and Moravec F (1996) Seasonal occurrence and maturation of Bathybothrium rectangulum (Cestoda: Amphycotilidae) in Barbus barbus (Pisces) of the Jihlava River, Czech Republic. Parasite 3, 39–44. PubMed

Schönhuth S, Vukić J, Šanda R, Yang L and Mayden RL (2018) Phylogenetic relationships and classification of the Holarctic family Leuciscidae (Cypriniformes: Cyprinoidei). Molecular Phylogenetics and Evolution 127, 781–799. PubMed

Šimková A, Desdevises Y, Gelnar M and Morand S (2000) Co-existence of nine gill ectoparasites (Dactylogyrus: Monogenea) parasitising the roach (Rutilus rutilus L.): history and present ecology. International Journal for Parasitology 30, 1077–1088. PubMed

Šimková A, Ondračková M, Gelnar M and Morand S (2002) Morphology and coexistence of congeneric ectoparasite species: reinforcement of reproductive isolation? Biological Journal of Linneean Society 76, 125–135.

Šimková A, Plaisance L, Matějusová I, Morand S and Verneau O (2003) Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridea): the need for the systematic revision of the Ancyrocephalinae Bychowsky, 1937. Systematic Parasitology 54, 1–11. PubMed

Šimková A, Morand S, Jobet E, Gelnar M and Verneau O (2004) Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): a case of intrahost speciation. Evolution 58, 1001–1018. PubMed

Šimková A, Verneau O, Gelnar M and Morand S (2006) Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution 60, 1023–1037. PubMed

Šimková A, Dávidová M, Papoušek I and Vetešník L (2013) Does interspecies hybridization affect the host specificity of parasites in cyprinid fish? Parasites & Vectors 6, 95. PubMed PMC

Šimková A, Řehulkova E, Jean Robertin R, Jorissen M, Scholz T, Faltynková A, Mašová S and Vanhove MPM (2018) Transmission of parasites from introduced tilapias: a new threat to endemic Malagasy ichthyofauna. Biological Invasions 21, 803–819.

Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England) 22, 2688–2690. PubMed

Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analyses and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313. PubMed PMC

Stefani F, Galli P, Crosa G, Zaccara S and Calamari D (2004) Alpine and Apennine barriers determining the differentiation of the rudd (Scardinius erythrophthalmus L.) in the Italian peninsula. Ecology of Freshwater Fish 13, 168–175.

Stout CC, Tan M, Lemmon AR, Lemmon EM and Armbruster JW (2016) Resolving Cypriniformes relationships using an anchored enrichment approach. BMC Evolutionary Biology 16, 244. PubMed PMC

Tan M and Armbruster JW (2018) Phylogenetic classification of extant genera of fishes of the order Cypriniformes (Teleostei: Ostariophysi). Zootaxa 4476, 6–39. PubMed

Thieltges DW, Hof C, Borregaard MK, Dehling DM, Brändle M, Brandl R and Poulin R (2011) Range size patterns in European freshwater trematodes. Ecography 34, 982–989.

van Maren MJ (1979) Structure and dynamics of the French upper Rhône ecosystems. XII. An inventar of helminth fish parasites from the upper Rhône river (France). Bulletin Zoological Museum 6, 189–200.

Verneau O, Du Preez L and Badets M (2009) Lessons from parasitic flatworms about evolution and historical biogeography of their vertebrate hosts. Comptes Rendus Biologies 332, 149–158. PubMed

Volta P, Jeppesen E, Sala P, Galafassi S, Foglini C, Puzzi C and Winfield IJ (2018) Fish assemblages in deep Italian subalpine lakes: history and present status with an emphasis on non-native species. Hydrobiologia 824, 255–270.

Waelbroeck C, Labeyrie L, Michel E, Duplessy JC, McManus JF, Lambeck K, Balbon E and Labracherie M (2002) Sea-level and deep water temperature changes derived from benthic foraminifera isotopic records. Quaternary Science Reviews 21, 295–305.

Wilson JR, Saunders RJ and Hutson KS (2019) Parasites of the invasive tilapia Oreochromis mossambicus: evidence for co-introduction. Aquatic Invasions 14, 332–349.

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