Species of Ergasilus von Nordmann, 1832 (Copepoda: Ergasilidae) from cichlid fishes in Lake Tanganyika

. 2023 Jun ; 150 (7) : 579-598. [epub] 20230320

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36938816

Ergasilus (von Nordmann, 1832) (Ergasilidae) is a species-rich group of parasitic copepods with a wide distribution in freshwater, marine and brackish environments. Up to now, 9 species of Ergasilus are known from cichlid fishes in Africa. In this study, 5 species, including 3 new, were collected from the gills of 12 cichlid species (11 genera: Bathybates, Ctenochromis, Eretmodus, Gnathochromis, Lamprologus, Neolamprologus, Ophthalmotilapia, Perissodus, Simochromis, Spathodus and Tanganicodus) of the northeastern shore of Lake Tanganyika in Burundi, namely E. macrodactylus (Sars, 1909), E. megacheir (Sars, 1909), E. caparti n. sp., E. parasarsi n. sp. and E. parvus n. sp. All species found were identified and described on the basis of adult female specimens using an integrative taxonomy approach mixing morphological characterization and molecular analyses of 2 ribosomal DNA markers (partial 18S and 28S rDNA sequences). An identification key for Ergasilus species from Lake Tanganyika is included. This study provides the first molecular data for Ergasilus species in Africa. The phylogenetic analyses suggest that the Ergasilus species parasitizing Lake Tanganyikan cichlids form a well-supported clade within the Ergasilidae. However, their phylogenetic relationships with other congeners still remain unclear due to a lack of molecular data for this diverse genus.

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Avenant-Oldewage A and Oldewage W (1993) Checklist of the parasitic Copepoda (Crustacea) of African fishes. Muséé Royal de l'Afrique Centrale Tervuren Belgique Documentation Zoologique 23, 1–28.

Baek SY, Jang KH, Choi EH, Ryu SH, Kim SK, Lee JH and Hwang UW (2016) DNA barcoding of metazoan zooplankton copepods from South Korea. PLoS ONE 11, 1–20. doi: 10.1371/journal.pone.0157307 PubMed DOI PMC

Boxshall GA and Defaye D (2007) Global diversity of copepods (Crustacea: Copepoda) in freshwater. In Balian EV, Lévêque C, Segers H and Martens K (eds), Freshwater Animal Diversity Assessment. Dordrecht: Springer Netherlands, pp. 195–207. doi: 10.1007/978-1-4020-8259-7_21 DOI

Boxshall GA and Halsey SH (2004) An Introduction to Copepod Diversity. London: Ray Society.

Boxshall GA and Montú MA (1997) Copepods parasitic on Brazilian coastal fishes: a handbook. Nauplius 5, 1–225.

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

Capart A (1944) Notes sur les Copépodes parasites. III. Copépodes parasites des poissons d'eau douce du Congo Belge. Bulletin du Musée Royal d'Histoire Naturelle de Belgique 20, 1–24.

Capart A (1956) Quelques Copepodes parasites de poissons du Niger (Gourao) recoltes par Th. Monod. Bulletin de l'Institut français d'Afrique noire (A) 18, 485–494.

Cohen AS, Soreghan MJ and Scholz CA (1993) Estimating the age of formation of lakes: an example from Lake Tanganyika, East African Rift system. Geology 21, 511.

Cunnington WA (1913) Zoological results of the third Tanganika expedition, conducted by Dr. W.A. Cunnington, 1904-1905: report on the Branchiura. Proceedings of the Zoological Society of London 37, 252–283.

Cunnington WA (1914) 45. Zoological results of die third Tanganyika expedition, conducted by Dr. W. A. Cuunington, 1904–1905: report on the parasitic Encopepoda. Proceedings of the Zoological Society of London 84, 819–829.

Cunnington WA (1920) 32. The fauna of the African lakes: a study in comparative limnology with special reference to Tanganyika. Proceedings of the Zoological Society of London 90, 507–622.

Darriba D, Taboada GL, Doallo R and Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772. PubMed PMC

Dávidová M and Smit N (2018) In: Scholz T, Vanhove MPM, Smit N, Jayasundera Z and Gelnar M (2018). A guide to the parasites of African freshwater fishes. Abc Taxa 18, 333–355.

Fischer C, Koblmüller S, Börger C, Michelitsch G, Trajanoski S, Schlötterer C, Guelly C, Thallinger GG and Sturmbauer C (2021) Genome sequences of Tropheus moorii and Petrochromis trewavasae, two eco-morphologically divergent cichlid fishes endemic to Lake Tanganyika. Scientific Reports 11, 4309. PubMed PMC

Folmer O, Hoeh WR, Black MB and Vrijenhoek RC (1994) Conserved primers for PCR amplification of mitochondrial DNA from different invertebrate phyla. Molecular Marine Biology and Biotechnology 3, 294–299. PubMed

Froese R and Pauly D (2022) FishBase. World Wide Web electronic publication, available from www.fishbase.org, 16 October 2022.

Fryer G (1956) A report on the parasitic Copepoda and Branchiura of the fishes of Lake Nyasa. Proceedings of the Zoological Society of London 127, 293–344.

Fryer G (1959) A report on the parasitic Copepoda and Branchiura of the fishes of Lake Bangweulu (Northern Rhodesia). Proceedings of the Zoological Society of London 132, 517–550.

Fryer G (1960) Studies on some parasitic crustaceans on African freshwater fishes, with descriptions of a new copepod of the genus Ergasilus and a new branchiuran of the genus Chonopeltis. Proceedings of the Zoological Society of London 133, 629–647.

Fryer G (1961) The parasitic Copepoda and Branchiura of the fishes of Lake Victoria and the Victoria Nile. Proceedings of the Zoological Society of London 137, 41–60.

Fryer G (1963) Crusatacean parasites from cichlid fishes of the genus Tilapia in the Musée Royal de l'Afrique central. Revue de Zoologie et de Botanique Africaines 68, 386–392.

Fryer G (1964) Further studies on the parasitic Crustacea of African freshwater fishes. Proceedings of the Zoological Society of London 143, 79–102.

Fryer G (1965) Crustacean parasites of African freshwater fishes, mostly collected during the expeditions to Lake Tanganika, and to Lakes Kivu, Edward and 91 Albert by the Institut Royal des Sciences Naturelles de Belgique. Bulletin Institut Royal des Sciences Naturelles de Belgique 41, 1–22.

Fryer G (1967) Parasitic copepods from African cichlids fishes in the Musée Royal de l'Afrique centrale. Revue de Zoologie et de Botanique Africaines 76, 357–363.

Fryer G (1968) The parasitic Crustacea of African freshwater fishes; their biology and distribution. Journal of Zoology 156, 45–95.

Gurney R (1928) Some Copepoda from Tanganyika collected by Mr. S. R. B. Pask. Proceedings of the Zoological Society of London 98, 317–332.

Hayward A, Tsuboi M, Owusu C, Kotrschal A, Buechel SD, Zidar J, Cornwallis CK, Løvlie H and Kolm N (2017) Evolutionary associations between host traits and parasite load: insights from Lake Tanganyika cichlids. Journal of Evolutionary Biology 30, 1056–1067. PubMed

Hoang DT, Chernomor O, von Haeseler A, Minh BQ and Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518–522. PubMed PMC

Huelsenbeck JP and Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755. PubMed

Huys R and Boxshall GA (1991) Copepod Evolution. London: Ray Society (Publications).

Huys R, Llewellyn-Hughes J, Olson PD and Nagasawa K (2006) Small subunit rDNA and Bayesian inference reveal Pectenophilus ornatus (Copepoda incertae sedis) as highly transformed Mytilicolidae, and support assignment of Chondracanthidae and Xarifiidae to Lichomolgoidea (Cyclopoida). Biological Journal of the Linnean Society 87, 403–425.

Irisarri I, Singh P, Koblmüller S, Torres-Dowdall J, Henning F, Franchini P, Fischer C, Lemmon AR, Lemmon EM, Thallinger GG, Sturmbauer C and Meyer A (2018) Phylogenomics uncovers early hybridization and adaptive loci shaping the radiation of Lake Tanganyika cichlid fishes. Nature Communications 9, 3159. PubMed PMC

Ivory SJ, McGlue MM, Peterman C, Baldwin P, Lucas J, Cohen A, Russell J, Saroni J, Msaky E, Kimirei I and Soreghan M (2021) Climate, vegetation, and weathering across space and time in Lake Tanganyika (tropical eastern Africa). Quaternary Science Advances 3, 100023.

Katoh K and Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780. PubMed PMC

Kilian E and Avenant-Oldewage A (2013) Infestation and pathological alterations by Ergasilus sarsi (Copepoda) on the Tanganyika Killifish from Africa. Journal of Aquatic Animal Health 25, 237–242. PubMed PMC

Kmentová N, van Steenberge M, Raeymaekers JAM, Koblmüller S, Hablützel PI, Bukinga FM, N'sibula TM, Mulungula PM, Nzigidahera B, Ntakimazi G, Gelnar M and Vanhove MPM (2018) Monogenean parasites of sardines in Lake Tanganyika: diversity, origin and intraspecific variability. Contributions to Zoology 87, 105–132.

Koblmüller S, Zangl L, Börger C, Daill D, Vanhove MPM, Sturmbauer C and Sefc KM (2019) Only true pelagics mix: comparative phylogeography of deepwater bathybatine cichlids from Lake Tanganyika. Hydrobiologia 832, 93–103. PubMed PMC

Kondo T and Hori M (1986) Abundance of zooplankters on a rocky shore of Lake Tanganyika: a preliminary report. African Study Monographs 6, 17–23.

Kvach Y, Tkachenko MY, Seifertová M and Ondračková M (2021) Insights into the diversity, distribution and phylogeny of three ergasilid copepods (Hexanauplia: Ergasilidae) in lentic water bodies of the Morava river basin, Czech Republic. Limnologica 91, 125922.

Marques TM, Boeger WA and de Carvalho Brasil-Sato M (2015) Two new species of Ergasilus Nordmann, 1832 (Copepoda: Ergasilidae) and a redescription of Ergasilus salmini Thatcher & Brazil-Sato, 2008 from Salminus brasiliensis Cuvier and S. franciscanus Lima & Britsky (Teleostei: Characidae) in Brazil. Systematic Parasitology 90, 81–89. PubMed

Marrone F, Lo Brutto S, Hundsdoerfer AK and Arculeo M (2013) Overlooked cryptic endemism in copepods: systematics and natural history of the calanoid subgenus Occidodiaptomus Borutzky 1991 (Copepoda, Calanoida. Diaptomidae). Molecular Phylogenetics and Evolution 66, 190–202. PubMed

Mayor TY, Galimova YA, Sheveleva NG, Sukhanova LV and Kirilchik SV (2017) Molecular phylogenetic analysis of Diacyclops and Acanthocyclops (Copepoda: Cyclopoida) from Lake Baikal based on COI gene. Russian Journal of Genetics 53, 252–258. PubMed

Miller MA, Pfeiffer W and Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In 2010 Gateway Computing Environments Workshop (GCE), pp. 1–8. IEEE. doi: 10.1109/GCE.2010.5676129 DOI

Morand S and Guégan J-F (2000) Patterns of endemism in host-parasite associations: lessons from epidemiological models and comparative tests. Belgian Journal of Entomology 2, 135–147.

Muriel-Hoyos F, Santana-Piñeros AM, Cruz-Quintana Y and Suárez-Morales E (2015) A new species of Ergasilus Nordmann, 1832 (Copepoda: Cyclopoida: Ergasilidae) from Bryconops giacopinii Fernández-Yépez (Characidae) in the Vichada River Basin, Colombia. Systematic Parasitology 92, 241–249. PubMed

Narciso RB, Brandão H, Perbiche-Neves G and da Silva RJ (2020) A new species of Rhinergasilus Boeger et Thatcher, 1988 (Copepoda: Ergasilidae) from gills of Astyanax fasciatus (Cuvier, 1819) (Actinopterygii: Characidae). Acta Parasitologica 65, 327–334. PubMed

Nguyen L-T, Schmidt HA, von Haeseler A and Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268–274. PubMed PMC

Oldewage WH and van As JG (1988) A key for the identification of African piscine parasitic Ergasilidae (Copepoda:Poecilostomatoida). South African Journal of Zoology 23, 42–46.

Oliveira MSB, Corrêa LL, Adriano EA and Tavares-Dias M (2021) Integrative taxonomy of a new species of Therodamas (Ergasilidae) infecting the Amazonian freshwater fish Leporinus fasciatus (Anostomidae). Parasitology Research 120, 3137–3147. PubMed

Ondračková M, Fojtů J, Seifertová M, Kvach Y and Jurajda P (2019) Non-native parasitic copepod Neoergasilus japonicus (Harada, 1930) utilizes non-native fish host Lepomis gibbosus (L.) in the floodplain of the River Dyje (Danube basin). Parasitology Research 118, 57–62. PubMed

Paperna ILAN (1969) Parasitic Crustacea from fishes of the Volta basin and South Ghana. Revue de Zoologie et de Botanique Africaines 80, 208–216.

Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, Sundberg 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

Raeymaekers JA, Hablützel PI, Grégoir AF, Bamps J, Roose AK, Vanhove MP, van Steenberge M, Pariselle A, Huyse T, Snoeks J and Volckaert FA (2013) Contrasting parasite communities among allopatric colour morphs of the Lake Tanganyika cichlid Tropheus. BMC Evolutionary Biology 13, 41. PubMed PMC

Raffini F, Fruciano C and Meyer A (2018) Morphological and genetic correlates in the left–right asymmetric scale-eating cichlid fish of Lake Tanganyika. Biological Journal of the Linnean Society 124, 67–84.

Rahmouni C, Vanhove MPM and Šimková A (2017) Underexplored diversity of gill monogeneans in cichlids from Lake Tanganyika: eight new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) from the northern basin of the lake, with remarks on the vagina and the heel of the male copulatory organ. Parasites & Vectors 10, 591. PubMed PMC

Rahmouni C, Vanhove MPM and Šimková A (2018) Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) parasitizing the gills of Congolese cichlids from northern Lake Tanganyika. PeerJ 6, e5604. PubMed PMC

Rambaut A (2012) FigTree v1.4.3 [Computer software]. Available from https://github.com/rambaut/figtree/releases, 15 April 2022.

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

Ronco F, Matschiner M, Böhne A, Boila A, Büscher HH, el Taher A, Indermaur A, Malinsky M, Ricci V, Kahmen A, Jentoft S and Salzburger W (2021) Drivers and dynamics of a massive adaptive radiation in cichlid fishes. Nature 589, 76–81. PubMed

Rushton-Mellor SK (1994a) The genus Argulus (Crustacea: Branchiura) in Africa: two new species, A. fryeri and A. gracilis, the previously undescribed male of A. brachypeltis Fryer and the identity of the male described as A. ambloplites Wilson. Systematic Parasitology 28, 23–31.

Rushton-Mellor SK (1994b) The genus Argulus (Crustacea: Branchiura) in Africa: redescriptions of type-material collected by W.A. Cunnington during the Lake Tanganyika Expedition in 1913, with notes on A. giganteus Lucas and A. arcassonensis Cuénot. Systematic Parasitology 28, 33–49.

Ryan EK, Soreghan MJ, McGlue MM, Todd JA, Michel E, Kaufman DS and Kimirei I (2020) Paleoenviromental implications of time-averaging and taphonomic variation of shell beds in Lake Tanganyika, Africa. PALAIOS 35, 49–66.

Santacruz A, Morales-Serna FN, Leal-Cardín M, Barluenga M and Pérez-Ponce de León G (2020) Acusicola margulisae n. sp. (Copepoda: Ergasilidae) from freshwater fishes in a Nicaraguan crater lake based on morphological and molecular evidence. Systematic Parasitology 97, 165–177. PubMed

Sars GOP (1909) Zoological results of the third Tanganyika expedition, conducted by Dr. W. A. Cunnington, F.Z.S., 1904–1905: report on the Copepoda. Proceedings of the Zoological Society of London 79, 31–77.

Satoh S, Ota K, Awata S and Kohda M (2019) Dynamics of sibling aggression of a cichlid fish in Lake Tanganyika. Hydrobiologia 832, 201–213.

Satoh S, Saeki T, Kohda M and Awata S (2022) Cooperative breeding in Neolamprologus bifasciatus, a cichlid fish inhabiting the deep reefs of Lake Tanganyika. Ecology of Freshwater Fish 31, 640–649. doi: 10.1111/eff.12658 DOI

Scholz T, Vanhove MPM, Smit N, Jayasundera Z and Gelnar M (2018) A Guide to the Parasites of African Freshwater Fishes. Brussels: Royal Belgian Institute of Natural Sciences, p. 424.

Shotter RA (1977) Copepod parasites of fishes from northern Nigeria. Bulletin de l'Institut fondamental d'Afrique noire 39, 583–600.

Smit N and Hadfield K (2018) In: Scholz T, Vanhove MPM, Smit N, Jayasundera Z and Gelnar M (2018). A guide to the parasites of African freshwater fishes. Abc Taxa 18, 333–355.

Snoeks J (2000) How well known is the ichthyodiversity of the large East African lakes?. Advances in Ecological Research 31, 17–38. doi: 10.1016/S0065-2504(00)31005-4 DOI

Song Y, Wang GT, Yao WJ, Gao Q and Nie P (2008) Phylogeny of freshwater parasitic copepods in the Ergasilidae (Copepoda: Poecilostomatoida) based on 18S and 28S rDNA sequences. Parasitology Research 102, 299–306. PubMed

Suárez-Morales E and Santana-Piñeros AM (2008) A new species of Ergasilus (Copepoda:Cyclopoida:Ergasilidae) from coastal fishes of the Mexican Pacific. Folia Parasitologica 55, 224–230. PubMed

Taborda NL, Paschoal F and Luque JL (2016) A new species of Ergasilus (Copepoda: Ergasilidae) from Geophagus altifrons and G. argyrostictus (Perciformes: Cichlidae) in the Brazilian Amazon. Acta Parasitologica 61, 549–555. doi: 10.1515/ap-2016-0073 PubMed DOI

Takahashi T (2003) Systematics of Tanganyikan cichlid fishes (Teleostei: Perciformes). Ichthyological Research 50, 367–382.

Takahashi T and Koblmüller S (2011) The adaptive radiation of cichlid fish in Lake Tanganyika: a morphological perspective. International Journal of Evolutionary Biology 2011, 1–14. PubMed PMC

Talavera G and Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577. PubMed

Tamura K, Stecher G and Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38, 3022–3027. PubMed PMC

Tang CQ, Leasi F, Obertegger U, Kieneke A, Barraclough TG and Fontaneto D (2012) The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proceedings of the National Academy of Sciences 109, 16208–16212. PubMed PMC

Taniguchi M, Kanehisa T, Sawabe T, Christen R and Ikeda T (2004) Molecular phylogeny of Neocalanus copepods in the subarctic Pacific Ocean, with notes on non-geographical genetic variations for Neocalanus cristatus. Journal of Plankton Research 26, 1249–1255.

Thurston JP (1970) The incidence of Monogenea and parasitic Crustacea on the gills of fish in Uganda. Revue de Zoologie et de Botanique Africaines 82, 111–130.

Trifinopoulos J, Nguyen L-T, von Haeseler A and Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44, W232–W235. PubMed PMC

van Douwe C (1912) Copepoda. Neue Süsswasser-Copepoden aus Südafrica. Zoolog, und Anthropol. Ergebnisse einer Forschungreise im westlichen u. zen tralen Südafrica in den Jahre 1908–1905 von Dr. Leonard Schultze. Systematik und Tiergeographie Lief 1, 23–32.

Vanhove MPM, Pariselle A, van Steenberge M, Raeymaekers JAM, Hablützel PI, Gillardin C, Hellemans B, Breman FC, Koblmüller S, Sturmbauer C, Snoeks J, Volckaert FAM and Huyse T (2015) Hidden biodiversity in an ancient lake: phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites. Scientific Reports 5, 13669. PubMed PMC

Varella AMB, Morey GAM and de Oliveira Malta JC (2019) Ergasilus tipurus n. sp. (Copepoda: Ergasilidae), a parasite of Brazilian Amazon fish species. Acta Parasitologica 64, 187–194. PubMed

Waicheim MA, Mendes Marques T, Rauque CA and Viozzi G (2021) New species of Ergasilus von Nordmann, 1832 (Copepoda: Ergasilidae) from the gills of freshwater fishes in Patagonia, Argentina. Systematic Parasitology 98, 131–139. PubMed

Wilson CB (1924) Parasitic copepods from the White Nile and the Red Sea. In Jägerskiöld ALKE (ed.), Results of the Swedish Zoological Expedition to Egypt and the White Nile, Vol. 5, 3 Uppsala: Royal University of Uppsala, pp. 1–17.

WoRMS Editorial Board (2022) World register of marine species. Available from https://www.marinespecies.org/ at VLIZ, 16 October 2022.

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