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Description of three new species of Gyrodactylus von Nordmann, 1832 (Monopisthocotylea: Gyrodactylidae) on Triplophysa species (Nemacheilidae) from Qinghai-Tibet Plateau

Published online by Cambridge University Press:  11 November 2024

X. Jin
Affiliation:
Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, P. R. China Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture (CAS), Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China
M. Li
Affiliation:
Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture (CAS), Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China University of Chinese Academy of Sciences, Beijing 100049, P. R. China
D. Zhang
Affiliation:
Key Laboratory of Biodiversity and Environment on the Qinghai-Tibetan Plateau, Ministry of Education and College of Ecology and Environmental Sciences, Tibet University, 850000, Lhasa, P. R. China.
H. Zou
Affiliation:
Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture (CAS), Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China
J. Cai
Affiliation:
Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, P. R. China
K. Amoah
Affiliation:
Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture, College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, P. R. China
G.T. Wang
Affiliation:
Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture (CAS), Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China University of Chinese Academy of Sciences, Beijing 100049, P. R. China
W.X. Li*
Affiliation:
Key Laboratory of Breeding Biotechnology and Sustainable Aquaculture (CAS), Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China University of Chinese Academy of Sciences, Beijing 100049, P. R. China
*
Corresponding author: Wenxiang Li; Email: [email protected]

Abstract

Three new species of Gyrodactylus were identified from the body surface of the Triplophysa species from the Qinghai-Tibet Plateau, Gyrodactylus triplorienchili n. sp. on Triplophysa orientalis in northern Tibet, G. yellochili n. sp. on T. sellaefer and T. scleroptera and G. triplsellachili n. sp. on T. sellaefer and T. robusta in Lanzhou Reach of the Yellow River. The three newly identified species share the nemachili group species’ characteristic of having inturning hamulus roots. Gyrodactylus triplorienchili n. sp. shared a quadrate sickle heel and a thin marginal hook sickle, two morphological traits that set them apart from G. yellochili n. sp. However, they may be identified by the distinct shapes of the sickle base and marginal hook sickle point. Gyrodactylus triplsellachili n. sp. had much larger opisthaptoral hard part size than the other two species. The three new species show relatively low interspecific differences of 2.9–5.3% p-distance for ITS1-5.85-ITS2 rDNA sequences. Phylogenetic analysis indicated that the three new species formed a well-supported monophyletic group (bp = 99) with the other nemachili group species.

Type
Research Paper
Copyright
© The Author(s), 2024. Published by Cambridge University Press

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References

Abdel-Latif, H.M.R., and Khafaga, A.F. (2020) Natural co-infection of cultured Nile tilapia Oreochromis niloticus with Aeromonas hydrophila and Gyrodactylus cichlidarum experiencing high mortality during summer. Aquaculture Research 51(5), 18801892. https://doi.org/10.1111/are.14538.CrossRefGoogle Scholar
Bakke, T.A., Cable, J., and Harris, P.D. (2007) The biology of gyrodactylid monogeneans: the “Russian-Doll Killers”. Advances in Parasitology 64, 161460. https://doi.org/10.1016/S0065-308X(06)64003-7.CrossRefGoogle Scholar
Boeger, W.A., Kritsky, D.C., and Pie, M.R. (2003). Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea). Zoologica Scripta 32, 437448. https://doi.org/10.1046/j.1463-6409.2003.00130-x.CrossRefGoogle ScholarPubMed
Christison, K.W., Shinn, A.P., and Van As, J.G. (2005) Gyrodactylus thlapi n. sp. (Monogenea) from Pseudocrenilabrus philander philander (Weber) (Cichlidae) in the Okavango Delta, Botswana. Systematic Parasitology 60(3), 165173. https://doi.org/10.1007/s11230-004-6342-x.CrossRefGoogle Scholar
Cunningham, C.O. (1997) Species variation within the internal transcribed spacer (ITS) region of Gyrodactylus (Monogenea: Gyrodactylidae) ribosomal RNA genes. The Journal of Parasitology 83(2), 215219. https://doi.org/10.2307/3284442.CrossRefGoogle Scholar
Dmitrieva, E., Sanna, D., Vodiasova, E., Prokhorova, D., Casu, M., Burreddu, C., Piras, M.C., Garippa, G., and Merella, P. (2022) Morphological and genetic variability of the cryptic Gyrodactylus sphinx and Gyrodactylus gerasevi n. sp. (Platyhelminthes: Monogenea) from the Mediterranean Sea and Black Sea: Two new members of the cross-ocean distributed Gyrodactylus orecchiae species group. Journal of Helminthology 96, e9. https://doi.org/10.1017/S0022149X21000778.CrossRefGoogle Scholar
Ergens, R. (1969) The suitability of ammonium picrate-glycerin in preparing slides of lower Monogenoidea. Folia Parasitologica 16, 320.Google Scholar
Ergens, R., and Allamuratov, A.B. (1972) Gyrodactylus karatagensis sp. n. (Monogenoidea) from the fins of Noemacheilus stoliczkai. Folia Parasitologica 19(2), 178178.Google Scholar
Ergens, R., and Bykhovsky, B.E. (1967) Revision of the species Gyrodactylus nemachili Bychowsky, 1936 (Monogenoidea). Folia Parasitologica 14(3), 225238.Google Scholar
Ergens, R., and Karabekova, D.U. (1980) Two new species of Gyrodactylus (Monogenea) from Kirghizian Diptychus dybowskii (Cypriniformes). Folia Parasitologica 27, 8991.Google Scholar
Ergens, R., and Kartunova, E.V. (1991) Gyrodactylus gvozdevi n. sp. (Gyrodactylidae: Monogenea) from Noemacheilus dorsalis (Kessler) in Kazakhstan. Systematic Parasitology 18(2), 117120. https://doi.org/10.1007/BF00017663.CrossRefGoogle Scholar
García-Vásquez, A., Hansen, H., Christison, K.W., Bron, J.E., and Shinn, A.P. (2011) Description of three new species of Gyrodactylus von Nordmann, 1832 (Monogenea) parasitising Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae). Acta Parasitologica 56(1), 2033. https://doi.org/10.2478/s11686-011-0005-2.CrossRefGoogle Scholar
Geets, A., Appleby, C., and Ollevier, F. (1999) Host-dependent and seasonal variation in opisthaptoral hard parts of Gyrodactylus cf. arcuatus from three Pomatoschistus spp. and G. arcuatus from Gasterosteus aculeatus: a multivariate approach. Parasitology 119(1), 2740. https://doi.org/10.1017/S0031182099004400.CrossRefGoogle Scholar
Gilmore, S.R., Cone, D.K., Lowe, G., King, S.K., Jones, S.R.M., and Abbott, C.L. (2012) Molecular phylogeny of Gyrodactylus (Monogenea) parasitizing fishes in fresh water, estuarine, and marine habitats in Canada. Canadian Journal of Zoology 90(6), 776786. https://doi.org/10.1139/Z2012-040.CrossRefGoogle Scholar
Harris, P.D., Bachmann, L., and Bakke, T.A. (2011) The parasites and pathogens of the Atlantic salmon: lessons from Gyrodactylus salaris. In Aas, Ø, Klemetsen, A, Einum, S and Skurdal, J (eds), Atlantic Salmon Ecology. Oxford, UK.: Blackwell Publishing Ltd., 221252.Google Scholar
Harris, P.D., Shinn, A.P., Cable, J., and Bakke, T.A. (2004) Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Systematic Parasitology 59(1), 127. https://doi.org/10.1023/B:SYPA.0000038447.52015. e4.CrossRefGoogle ScholarPubMed
Huyse, T., Audenaert, V., and Volckaert, F.A.M. (2003) Speciation and host–parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei). International Journal for Parasitology 33(14), 16791689. https://doi.org/10.1016/S0020-7519(03)00253-4.CrossRefGoogle ScholarPubMed
Huyse, T., and Volckaert, F.A.M. (2002) Identification of a host-associated species complex using molecular and morphometric analyses, with the description of Gyrodactylus rugiensoides n. sp. (Gyrodactylidae, Monogenea). International Journal for Parasitology 32(7), 907919. https://doi.org/10.1016/S0020-7519(02)00026-7.CrossRefGoogle Scholar
Jin, X., Li, W., Cheng, Y., Li, M., Wu, S., Zou, H., and Wang, G. (2022) Description of Gyrodactylus banmae n. sp. (Monogenea, Gyrodactylidae) parasitic on zebrafish, Danio rerio. Parasitology International 87, 102531. https://doi.org/10.1016/j.parint.2021.102531.CrossRefGoogle Scholar
Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A., and Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14(6), 587589. https://doi.org/10.1038/nmeth.4285.CrossRefGoogle ScholarPubMed
Kritsky, C.D., Ali, H.A., and Khamees, R.N. (2013) Gyrodactylus aff. mugili Zhukov, 1970 (Monogenoidea: Gyrodactylidae) from the gills of mullets (Mugiliformes: Mugilidae) collected from the inland waters of southern Iraq, with an evaluation of previous records of Gyrodactylus spp. on mullets in Iraq. Folia Parasitologica 60(5), 441447. https://doi.org/10.14411/fp.2013.047.CrossRefGoogle Scholar
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35(6), 15471549. https://doi.org/10.1093/molbev/msy096.CrossRefGoogle ScholarPubMed
Lebedeva, D., Muñoz, G., and Lumme, J. (2021) New salinity tolerant species of Gyrodactylus (Platyhelminthes, Monogenea) on intertidal and supratidal fish species from the Chilean coast. Acta Parasitologica 66(3), 10211030. https://doi.org/10.1007/s11686-021-00347-x.CrossRefGoogle ScholarPubMed
Lebedeva, D., Ziętara, M., Mendsaikhan, B., Ermolenko, A., and Lumme, J. (2023) Survivors from a Pliocene climatic catastrophe: Gyrodactylus (Platyhelminthes, Monogenea) parasites of the relict fishes in the Central Asian Internal drainage basin of Mongolia. Diversity 15(7), 860. https://doi.org/10.3390/d15070860.CrossRefGoogle Scholar
Li, J., Wang, Y., Jin, H., Li, W., Yan, C., Yan, P., Zhang, X., He, S., and Song, Z. (2017) Identification of Triplophysa species from the Qinghai-Tibetan Plateau (QTP) and its adjacent regions through DNA barcodes. Gene 605, 1219. https://doi.org/10.1016/j.gene.2016.11.045.CrossRefGoogle ScholarPubMed
Li, R., Li, W., Wu, X., and Wang, G. (2014) Identification of Gyrodactylus species in goldfish (Carassius auratus) through morphological study and the analysis of the rDNA ITS sequence. Acta Hydrobiologica Sinica 38, 903909. https://doi.org/10.7541/2014.135Google Scholar
Lumme, J., Ziętara, M.S., and Lebedeva, D. (2017) Ancient and modern genome shuffling: Reticulate mito-nuclear phylogeny of four related allopatric species of Gyrodactylus von Nordmann, 1832 (Monogenea: Gyrodactylidae), ectoparasites on the Eurasian minnow Phoxinus phoxinus (L.) (Cyprinidae). Systematic Parasitology 94(2), 183200. https://doi.org/10.1007/s11230-016-9696-y.CrossRefGoogle ScholarPubMed
Luton, K., Walker, D., and Blair, D. (1992) Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology 56(2), 323327. https://doi.org/10.1016/0166-6851(92)90181-I.CrossRefGoogle ScholarPubMed
Malmberg, G. (1970) The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv for Zoologie 23, 1237.Google Scholar
Matejusová, I., Gelnar, M., McBeath, A.J.A., Collins, C.M., and Cunningham, C.O. (2001) Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). International Journal for Parasitology 31(7), 738745. https://doi.org/10.1016/S0020-7519(01)00176-X.CrossRefGoogle ScholarPubMed
Matejusová, I., Gelnar, M., Verneau, O., Fraser, C., and Littlewood, D.T.J. (2003) Molecular phylogenetic analysis of the genus Gyrodactylus (Platyhelminthes: Monogenea) inferred from rDNA ITS region: subgenera versus species groups. Parasitology 127, 603611. https://doi.org/10.1017/S0031182003004098.CrossRefGoogle ScholarPubMed
Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., Von Haeseler, A., and Lanfear, R. (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37(5), 15301534. https://doi.org/10.1093/molbev/msaa015.CrossRefGoogle ScholarPubMed
Mo, T.A. (1991) Variations of opisthaptoral hard parts of Gyrodactylus salaris Malmberg, 1957 (Monogenea: Gyrodactylidae) on rainbow trout Oncorhynchus mykiss (Walbaum, 1792) in a fish farm, with comments on the spreading of the parasite in south-eastern Norway. Systematic Parasitology 20(1), 19. https://doi.org/10.1007/BF00009706.CrossRefGoogle Scholar
Mo, T.A. (1993) Seasonal variations of the opisthaptoral hard parts of Gyrodactylus derjavini Mikailov, 1975 (Monogenea: Gyrodactylidae) on brown trout Salmo trutta L. parr and Atlantic salmon S. salar L. parr in the River Sandvikselva, Norway. Systematic Parasitology 26(3), 225231. https://doi.org/10.1007/BF00009730.CrossRefGoogle Scholar
Nakamura, T., Yamada, K.D., Tomii, K., and Katoh, K. (2018) Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 34(14), 24902492. https://doi.org/10.1093/bioinformatics/bty121.CrossRefGoogle ScholarPubMed
Nitta, M. (2021) A new monogenean species, Gyrodactylus ajime n. sp. (Gyrodactylidae), parasitic on Niwaella delicata (Niwa), an endemic loach of Japan. Systematic Parasitology 98(3), 307319. https://doi.org/10.1007/s11230-021-09979-z.Google ScholarPubMed
Paladini, G., Cable, J., Fioravanti, L.M., Faria, J.P., Di Cave, D., and Shinn, P.A. (2009) Gyrodactylus orecchiae sp. n. (Monogenea: Gyrodactylidae) from farmed populations of gilthead seabream (Sparus aurata) in the Adriatic Sea. Folia Parasitologica 56(1), 2128. https://doi.org/10.14411/fp.2009.004.CrossRefGoogle Scholar
Peng, Z., Ho, S.Y.W., Zhang, Y., and He, S. (2006) Uplift of the Tibetan plateau: Evidence from divergence times of glyptosternoid catfishes. Molecular Phylogenetics and Evolution 39(2), 568572. https://doi.org/10.1016/j.ympev.2005.10.016.CrossRefGoogle ScholarPubMed
Pinacho-Pinacho, C.D., Calixto-Rojas, M., García-Vásquez, A., Guzmán-Valdivieso, I., Barrios-Gutiérrez, J.J., and Rubio-Godoy, M. (2021) Species delimitation of Gyrodactylus (Monogenea: Gyrodactylidae) infecting the southernmost cyprinids (Actinopterygii: Cyprinidae) in the New World. Parasitology Research 120(3), 831848. https://doi.org/10.1007/s00436-020-06987-8.CrossRefGoogle Scholar
Přikrylová, I., Matějusová, I., Jarkovský, J., and Gelnar, M. (2008) Morphometric comparison of three members of the Gyrodactylus nemachili-like species group (Monogenea: Gyrodactylidae) on Barbatula barbatula L . in the Czech Republic, with a reinstatement of G. papernai Ergens & Bychowsky, 1967. Systematic Parasitology 69(1), 3344. https://doi.org/10.1007/s11230-007-9106-6.Google ScholarPubMed
Pugachev, O.N., Gerasev, P.I., Gussev, A.V., Ergens, R., and Khotenowsky, I. (2009) Guide to Monogenoidea of freshwater fish of Palaeartic and Amur regions. Milan: Ledizione-Ledi Publishing.Google Scholar
R Core, Team (2017) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rahmouni, C., Seifertová, M., and Šimková, A. (2023) Revealing the hidden diversity of Gyrodactylus communities (Monogenea, Gyrodactylidae) from Nearctic Catostomidae and Leuciscidae fish hosts (Teleostei, Cypriniformes), with descriptions of ten new species. Parasite 30, 40. https://doi.org/10.1051/parasite/2023035.CrossRefGoogle ScholarPubMed
Razo-Mendivil, U., García-Vásquez, A., and Rubio-Godoy, M. (2016) Spot the difference: Two cryptic species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) infecting Astyanax aeneus (Actinopterygii, Characidae) in Mexico. Parasitology International 65(5, Part A), 389400. https://doi.org/10.1016/j.parint.2016.05.009.CrossRefGoogle Scholar
Sheraliev, B., and Peng, Z. (2021) Triplophysa ferganaensis, a new loach species from Fergana Valley in Central Asia (Teleostei: Nemacheilidae). Journal of Fish Biology 99, 807817. https://doi.org/10.1111/jfb.14764.CrossRefGoogle ScholarPubMed
Shinn, A.P., des Clers, S., Gibson, D.I., and Sommerville, C. (1996) Multivariate analyses of morphometrical features from Gyrodactylus spp. (Monogenea) parasitising British salmonids: Light microscope based studies. Systematic Parasitology 33(2), 115125. https://doi.org/10.1007/BF00009427.CrossRefGoogle Scholar
Shinn, A.P., Hansen, H., Olstad, K., Bachmann, L., and Bakke, T.A. (2004) The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasitologica 51(2), 239252. https://doi.org/10.14411/fp.2004.029.CrossRefGoogle Scholar
Talavera, G., and Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56(4), 564577. https://doi.org/10.1080/10635150701472164.CrossRefGoogle ScholarPubMed
Tang, Q., Liu, H., Mayden, R., and Xiong, B. (2006) Comparison of evolutionary rates in the mitochondrial DNA cytochrome b gene and control region and their implications for phylogeny of the Cobitoidea (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution 39(2), 347357. https://doi.org/10.1016/j.ympev.2005.08.007.CrossRefGoogle ScholarPubMed
Wang, T., Zhang, Y., Yang, Z., Liu, Z., and Du, Y. (2020) DNA barcoding reveals cryptic diversity in the underestimated genus Triplophysa (Cypriniformes: Cobitidae, Nemacheilinae) from the northeastern Qinghai-Tibet Plateau. BMC Evolutionary Biology 20(1), 151. https://doi.org/10.1186/s12862-020-01718-0.CrossRefGoogle ScholarPubMed
Wang, Y., Shen, Y., Feng, C., Zhao, K., Song, Z., Zhang, Y., Yang, L., and He, S. (2016) Mitogenomic perspectives on the origin of Tibetan loaches and their adaptation to high altitude. Scientific Reports 6, 29690. https://doi.org/10.1038/srep29690.CrossRefGoogle ScholarPubMed
Wu, Y., and Tan, Q. (1991) Characteristic of the fish-fauna of the characteristic of Qinghai-Xizang Plateau and its geological distribution and formation. Acta Zoologica Sinica 37(02), 135152.Google Scholar
Xiang, C., Gao, F., Ivan, J., Lei, H., He, Y., Zhang, H., Zou, H., Wang, G., and Zhang, D. (2023) Using PhyloSuite for molecular phylogeny and tree-based analyses. iMeta 2(1), e87. https://doi.org/10.1002/imt2.87.CrossRefGoogle ScholarPubMed
Zhang, D., Gao, F., Ivan, J., Zou, H., Zhang, J., Li, W., and Wang, G. (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources 20(1), 348355. https://doi.org/10.1111/1755-0998.13096.CrossRefGoogle ScholarPubMed
Zhang, W., Hao, C., Arken, K., Rong, M., Tian, S., Kadir, M., and Yue, C. (2023) New species of Gyrodactylus von Nordmann, 1832 (Monogenoidea: Gyrodactylidae) from Gymnodiptychus dybowskii (Kessler, 1874) (Schizothoracinae) in the Kunes River (Yili River basin), China. International Journal for Parasitology : Parasites and Wildlife 22, 136145. https://doi.org/10.1016/j.ijppaw.2023.10.002.CrossRefGoogle Scholar
Zheng, L., Du, L., Chen, X., and Yang, J. (2009) A new species of genus Triplophysa (Nemacheilinae: Balitoridae), Triplophysa longipectoralis sp. nov, from Guangxi, China. Environmental Biology of Fishes 85, 221227. https://doi.org/10.1007/s10641-009-9485-4.CrossRefGoogle Scholar
Ziętara, M.S., Lebedeva, D., Muñoz, G., and Lumme, J. (2012) A monogenean fish parasite, Gyrodactylus chileani n. sp., belonging to a novel marine species lineage found in the South-Eastern Pacific and the Mediterranean and North Seas. Systematic Parasitology 83(2), 159167. https://doi.org/10.1007/s11230-012-9379-2.CrossRefGoogle Scholar
Ziętara, M.S., and Lumme, J. (2002) Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution 56(12), 24452458. https://doi.org/10.1111/j.0014-3820.2002.tb00170.x.Google Scholar
Ziętara, M.S., and Lumme, J. (2003) The crossroads of molecular, typological and biological species concepts: two new species of Gyrodactylus Nordmann, 1832 (Monogenea: Gyrodactylidae). Systematic Parasitology 55(1), 3952. https://doi.org/10.1023/A:1023938415148.CrossRefGoogle ScholarPubMed
Ziętara, M.S., and Lumme, J. (2004) Comparison of molecular phylogeny and morphological systematics in fish parasite genus Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). Zoologica Poloniae 49, 528.Google Scholar
Ziętara, M.S., Kuusela, J., Veselov, A., and Lumme, J. (2008). Molecular faunistics of accidental infections of Gyrodactylus Nordmann, 1832 (Monogenea) parasitic on salmon Salmo salar L. and brown trout Salmo trutta L. in NW Russia. Systematic Parasitology 69, 123135. https://doi.org/10.1007/s11230-007-9121-7.CrossRefGoogle Scholar