Abstract
Species of the genus Ceriodaphnia Dana, 1853 (Crustacea: Cladocera: Daphniidae) are present in the plankton of many freshwater bodies all around the World. However, the taxonomy of the genus is still poorly developed. Most species have been described in the nineteenth century and data on their morphology and distribution should be revised according to current standards. Currently, due to lack of reliable morphological and genetic data, almost all nominal species of Ceriodaphnia are considered as species groups rather than separate biological species, complicating the detection and description of new species of the genus. Here, we redescribe the morphology of Ceriodaphnia quadrangula (O.F. Müller, 1785) based on material close to the type locality in Denmark, and describe a new species of Ceriodaphnia from the Mediterranean region. Also, we provide a phylogenetic analysis using existing and novel sequences of mitochondrial DNA of the commonest species of the genus. Ceriodaphnia smirnovi sp. nov. can be easily distinguished from C. quadrangula via presence of the head pore and the structure of the second thoracic limb, the postabdomen and the ephippium. From other species of Ceriodaphnia known to date C. smirnovi sp. nov. can also be separated on ephippium structure and some other fine morphological features. Although distribution range of C. smirnovi sp. nov. must be clarified in the future based on analysis of more sampling points, most likely, it is restricted to the Mediterranean region. The phylogenetic analyses showed high divergence among 16 different clades (mean clade separation of 13±2.3 % (mean ± SD) and 20.7±2.1% for 16S and COI respectively). These clades belonged to 11 described species and 5 undescribed. The high intraspecific variability of some species indicates the possible existence of more undescribed species within present species groups.
References
Abell, R., Thieme, M.L., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Balderas, S.C., Bussing, W., Stiassny, M.L.J., Skelton, P., Allen, G.R., Unmack, P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., Higgins, J.V., Heibel, T.J., Wirkamanayake, E., Olson, D., López, H.L., Reis, R.E., Lundberg, J.G., Sabaj Pérez, M. & Petry, P. (2008) Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. BioScience, 58, 403–414.
https://doi.org/10.1641/B580507
Abreu, M.J., Santos-Wisniewski, M.J., Rocha, O. & Orlando, T.C. (2010) The use of PCR-RFLP to genetically distinguish themorphologically close species: Ceriodaphnia dubia Richard, 1894 and Ceriodaphnia silvestrii Daday, 1902 (Crustacea, Cladocera). Brazilian Journal of Biology, 70, 121–124.
https://doi.org/10.1590/S1519-69842010000100016
Abreu, C.B. de (2016) Diversidade genética de cladocera (Crustacea: Branchiopoda) do Sul de Minas Gerais, utilizando DNA Barcode como marcador molecular. MSc dissertation. Instituto de Ciências da Natureza. Universidade Federal de Alfenas, Alfenas, Poços de Caldas and Varginha, 83 pp.
Alonso, M. (1991) Review of Iberian Cladocera with remarks on ecology and biogeography. Hydrobiologia, 225 (1), 37–43.
https://doi.org/10.1007/BF00028383
Alonso, M. (1996) Crustacea Branchiopoda. In: Ramos, M. (Ed.), Fauna Ibérica. Museo Nacional de Ciencias Naturales. Consejo Superior de Investigaciones Científicas, Madrid, 7, 1–486.
Alonso, M. &Pretus, J.L. (1989) Alona iberica, new species: first evidence of Noncosmopolitanism within the A. karua complex (Cladocera, Chydoridae). Journal of Crustacean Biology, 9 (3), 459–476. https://doi.org/10.1163/193724089X00449
Alonso, M., Neretina, A.N., Sanoamuang, L.O., Saengphan, N. & Kotov, A.A. (2019) A new species of Moina Baird, 1850 (Cladocera: Moinidae) from Thailand. Zootaxa, 4554 (1), 199–218.
https://doi.org/10.11646/zootaxa.4554.1.6
Bhavan, P. S., R. Udayasuriyan, C. Vadivalagan, R. Kalpana and S. Umamaheswari (2016) Diversity of zooplankton in four perennial lakes of Coimbatore (India) and molecular characterization of Asplanchna intermedia, Moina micrura, Mesocyclops edax and Cypris protubera through mt-COI gene. Journal of Entomology and Zoology Studies, 4 (2), 183–197. [https://www.entomoljournal.com/archives/2016/vol4issue2/PartC/4-2-16.pdf]
Bekker, E.I., Karabanov, D.P., Galimov, Y.R. & Kotov, A.A. (2016) DNA barcoding reveals high cryptic diversity in the North Eurasian Moina species (Crustacea: Cladocera). PloS ONE, 11 (8), e0161737.
https://doi.org/10.1371/journal.pone.0161737
Bekker, E.I., Karabanov, D.P., Galimov, Y.R., Haag, C.R., Neretina, T.V. & Kotov, A.A. (2018) Phylogeography of Daphnia magna Straus (Crustacea: Cladocera) in Northern Eurasia: evidence for a deep longitudinal split between mitochondrial lineages. PloS one, 13 (3), e0194045.
https://doi.org/10.1371/journal.pone.0194045
Berner, D.B. (1985) Morphological differentiation among species in the Ceriodaphnia cornuta complex (Crustacea, Cladocera). Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie, 22, 3099–3103.
https://doi.org/10.1080/03680770.1983.11897839
Berner, D.B. (1986) Taxonomy of Ceriodaphnia (Crustacea: Cladocera) in U.S. Environmental Protection Agency Cultures.U.S. Environmental Protection Agency, Cincinnati, 34 pp.
Berner, D.B. (1987) Significance of head and carapace pores in Ceriodaphnia (Crustacea, Cladocera). Hydrobiologia, 145, 75–84.
https://doi.org/10.1007/BF02530267
Berner, D.B. (1992) Restricted distribution of Ceriodaphnia quadrangula in North America. XXV SIL International Congress, Memorias, 1, 50.
Berner, D.B. & Rahmatullayeva, G. (2001) A new species of Ceriodaphnia from Uzbekistan and Kazakhstan. Hydrobiologia, 442, 29–39.
https://doi.org/10.1023/A:1017586106850
Bilton, D.T., Mirol, P.M., Mascheretti, S., Fredga, K., Zima, J. & Searle, J.B. (1998) Mediterranean Europe as an area of endemism for small mammals rather than a source for northwards postglacial colonization. Proceedings of the Royal Society of London. Series B: Biological Sciences, 265 (1402), 1219–1226.
https://doi.org/10.1098/rspb.1998.0423
Brehm, V. (1950) Marokkanische Cladoceren. Bulletin de la Société de Sciences naturelles du Maroc, Rabat, 30, 33–35.
Carranza, S. & Amat, F. (2005) Taxonomy, biogeography and evolution of Euproctus (Amphibia: Salamandridae), with the resurrection of the genus Calotriton and the description of a new endemic species from the Iberian Peninsula. Zoological Journal of the Linnean Society, 145 (4), 555–582.
https://doi.org/10.1111/j.1096-3642.2005.00197.x
Chiambeng, G.Y. & Dumont, H.J. (2005) The Branchiopoda (Crustacea: Anomopoda, Ctenopoda and Cyclestherida) of the rain forests of Cameroon, West Africa: low abundances, few endemics and a boreal-tropical disjunction. Journal of Biogeography, 32, 1611–1620.
https://doi.org/10.1111/j.1365-2699.2005.01280.x
deWaard, J R., Sacherova, V., Cristescu, M.E., Remigio, E.A., Crease, T.J. & Hebert, P.D. (2006) Probing the relationships of the branchiopod crustaceans. Molecular Phylogenetics and Evolution, 39 (2), 491–502.
https://doi.org/10.1016/j.ympev.2005.11.003
Domingos, A.R. (2018) Zooplanctofagia de heterópteros na estrutura da comunidade zooplanctônica em um lago neotropical: análise integrada entre DNA do conteúdo alimentar e experimento em mesocosmo, Universidade de São Paulo. 161737.
https://doi.org/10.11606/T.59.2019.tde-11032019-155957
Dumont, H.J., Laureys, P. & Pensaert, J. (1979) Anostraca, Conchostraca, Cladocera and Copepoda from Tunisia. Hydrobiologia, 66 (3), 259–274.
https://doi.org/10.1007/BF00020908
Elias-Gutierrez, M., Jeronimo, F.M., Ivanova, N.V., Valdez-Moreno, M. & Hebert, P.D.N. (2008) DNA barcodes for Cladocera and Copepoda from Mexico and Guatemala, highlights and new discoveries. Zootaxa, 1839 (1), 1–42.
https://doi.org/10.11646/zootaxa.1839.1
Elías-Gutiérrez, M., Valdez-Moreno, M., Topan, J., Young, M.R. & Cohuo-Colli, J.A. (2018) Improved protocols to accelerate the assembly of DNA barcode reference libraries for freshwater zooplankton. Ecology and Evolution, 8 (5), 3002–3018. https://doi.org/10.1002/ece3.3742
Flössner, D. (2000) Die Haplopoda und Cladocera (ohne Bosminidae) Mitteleuropas. Backhuys, Leiden, 428 pp.
Frey, D.G. (1980) The non-swimming chydorid Cladocera of wet forests, with descriptions of a new genus and two new species. Internationale Revue der gesamten Hydrobiologie und Hydrographie, 65 (5), 613–641.
https://doi.org/10.1002/iroh.19800650502
Ghaouaci, S., Amarouayache, M., Sinev, A.Y., Korovchinsky, N.M. & Kotov, A.A. (2018) An annotated checklist of the Algerian Cladocera (Crustacea: Branchiopoda). Zootaxa, 4377 (3), 412–430.
https://doi.org/10.11646/zootaxa.4377.3.5
Geller, J., Meyer, C., Parker, M. & Hawk, H. (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Molecular Ecology Resources, 13, 851–861.
https://doi.org/10.1111/1755-0998.12138
Gu, L., Qin, S., Zhu, S., Lu, N., Sun, Y., Zhang, L., Huang, Y., Lyu, K., Chen, Y. & Yang, Z. (2020) Microcystis aeruginosa affects the inducible anti-predator responses of Ceriodaphnia cornuta. Environmental Pollution, 259, 11395.
https://doi.org/10.1016/j.envpol.2020.113952
Guareschi, S., Mellado-Díaz, A., Puig, M.Á. & Sánchez-Fernández, D. (2018) On the Iberian endemism Eurylophella iberica Keffermuller and Da Terra 1978 (Ephemeroptera, Ephemerellidae): current and future potential distributions, and assessment of the effectiveness of the Natura 2000 network on its protection. Journal of insect conservation, 22 (1), 127–134.
https://doi.org/10.1007/s10841-018-0044-1
Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321. https://doi.org/10.1093/sysbio/syq010
Gurney, R. (1909) On the freshwater Crustacea of Algeria and Tunisia. Journal of the Royal Microscopical Society, 2, 273–305.
https://doi.org/10.1111/j.1365-2818.1909.tb01699.x
Hudec, I. (2010) Anomopoda, Ctenopoda, Haplopoda, Onychopoda (Crustacea: Branchiopoda). Fauna Slovenska III. VEDA, Bratislava, 496 pp.
Hebert, P.D., Ratnasingham, S. & de Waard, J.R. (2003) Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B: Biological Sciences, 270 (Supplement 1), S96–S99.
https://doi.org/10.1098/rsbl.2003.0025
Jeffery, N.W., Elías-Gutiérrez, M. & Adamowicz, S.J. (2011) Species diversity and phylogeographical affinities of the Branchiopoda (Crustacea) of Churchill, Manitoba, Canada. PLoS One, 6 (5), e18364.
https://doi.org/10.1371/journal.pone.0018364
Jiang, X., Xie, J., Xu, Y., Zhong, W., Zhu, X. & Zhu, C. (2017) Increasing dominance of small zooplankton with toxic cyanobacteria. Freshwater Biology, 62 (2), 429–443.
https://doi.org/10.1111/fwb.12877
Jurine, L. (1820) Histoire des Monocies, quise trouvent aux environs de Genève. Paschoud, Genf & Paris, 260 pp.
https://doi.org/10.5962/bhl.title.10137
Korovchinsky, N.M. (1995) Ceriodaphnia (Daphniidae) In: Alexeev, V.R. (Ed.), Key book for freshwater invertebrates of Russia and surrounding territories. Vol. 2. Crustacea. KMK, Moscow, pp. 47–48.
Korovchinsky, N.M. (2006) The Cladocera (Crustacea: Branchiopoda) as a relict group. Zoological Journal of the Linnean Society, 147 (1), 109–124.
https://doi.org/10.1111/j.1096-3642.2006.00217.x
Kotov, A.A. (2013) Morphology and phylogeny of Anomopoda (Crustacea: Cladocera). KMK, Moscow, 638 pp. [in Russian with English abstract]
Kotov, A.A. & Alonso, M. (2010) Two new species of Leydigia Kurz, 1875 (Chydoridae, Cladocera) from Spain. Zootaxa, 2673 (1), 39–55.
https://doi.org/10.11646/zootaxa.2673.1.2
Kotov, A.A. & Taylor, D.J. (2019) Contrasting endemism in pond-dwelling cyclic parthenogens: the Daphnia curvirostris species group (Crustacea: Cladocera). Scientific Reports, 9 (1), 6812.
https://doi.org/10.1038/s41598-019-43281-9
Kotov, A.A., Ibragimova, A.G. & Neretina, A.N. (2018) Identification of Ceriodaphnia Dana, 1853 (Crustacea: Cladocera) taxa from European Russia based on ephippial morphology. Zootaxa, 4527 (1), 105–123.
https://doi.org/10.11646/zootaxa.4527.1.9
Kotov, A.A., Sinev, A.Y., Glagolev, S.M. & Smirnov, N.N. (2010) Water fleas (Cladocera). In: Alexeev, V.R. & Tsalolokhin, S.Y. (Eds.), Key book for zooplankton and zoobenthos of fresh waters of European Russia. KMK, Moscow, pp. 151–276.
Kotov, A.A., Forró, L., Korovchinsky, N.M. & Petrusek, A. (2013) World checklist of freshwater Cladocera species. World Wide Web electronic publication. Available from: http://fada.biodiversity.be/group/show/17 (accessed 30 August 2019)
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular biology and evolution, 33, 1870–1874.
https://doi.org/10.1093/molbev/msw054
Laforsch, C. & Tollrian, R. (2000) A new preparation technique of daphnids for Scanning Electron Microscopy usinghexamethyldisilazane. Archiv für Hydrobiologie, 149, 587–596.
https://doi.org/10.1127/archiv-hydrobiol/149/2000/587
Lampert, W. (2011) Daphnia: development of a model organism in ecology and evolution. Excellence in Ecology, 21, 1–250.
Lilljeborg, W. (1901) Cladocera Sueciae. Nova acta regiae societatis scientatis scientiarum upsaleinsis, Seriei Tertiae, 19, 1–701.
Makino, W., Maruoka, N., Nakagawa, M. & Takamura, N. (2017) DNA barcoding of freshwater zooplankton in Lake Kasumigaura, Japan. Ecological Research, 32 (4), 481–493.
https://doi.org/10.1007/s11284-017-1458-z
Marrone, F., Alfonso, G., Stoch, F., Pieri, V., Alonso, M., Dretakis, M. & Naselli-Flores, L. (2019) An account on the non-malacostracan crustacean fauna from the inland waters of Crete, Greece, with the synonymization of Arctodiaptomus piliger Brehm, 1955 with Arctodiaptomus alpinus (Imhof, 1885) (Copepoda: Calanoida). Limnetica, 38 (1), 167–187.
https://doi.org/10.23818/limn.38.01
Matile, P. (1890) Die Cladocera der Umgegend von Moscou. Bulletin de la Société Impériale des naturalistes de Moscou, 1 (for 1890), 1–67.
Médail, F. & Diadema, K. (2009) Glacial refugia influence plant diversity patterns in the Mediterranean Basin. Journal of Biogeography, 36 (7), 1333–1345.
https://doi.org/10.1111/j.1365-2699.2008.02051.x
Montero-Pau, J., Gomez, A. & Munoz, J. (2008) Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnology and Oceanography-Methods, 6, 218–222.
https://doi.org/10.4319/lom.2008.6.218
Müller, O.F. (1785) Entomostraca seu Insecta Testacea, quae in aquis Daniae et Norvegiae reperit, descripsit et iconibus illustravit. Symtibus Bibliopolii J.G. Mülleriani, Lipsiae et Havniae (Leipzig and Copenhagen), 135 pp.
https://doi.org/10.5962/bhl.title.14414
Ni, Y., Ma, X., Hu, W., Blair, D. & Yin, M. (2019) New lineages and old species: Lineage diversity and regional distribution of Moina (Crustacea: Cladocera) in China. Molecular Phylogenetics and Evolution, 134, 87–98.
https://doi.org/10.1016/j.ympev.2019.02.007
Ott, J. (2001) Expansion of Mediterranean Odonata in Germany and Europe— consequences of climatic changes. In: Walther, G.-R., Burga, C.A. & Edwards, P.J. (Eds.), “Fingerprints” of Climate Change. Springer, Boston, pp. 89–111.
https://doi.org/10.1007/978-1-4419-8692-4_6
Palumbi, S.R. (1996) What can molecular genetics contribute to marine biogeography? An urchin’s tale. Journal of Experimental Marine Biology and Ecology, 203, 75–92.
https://doi.org/10.1016/0022-0981(96)02571-3
Prosser, S., Martínez-Arce, A. & Elías-Gutiérrez, M. (2013) A new set of primers for COI amplification from freshwater microcrustaceans. Molecular Ecology Resources, 13 (6), 1151–1155.
https://doi.org/10.1111/1755-0998.12132
Posada, D. (2008) jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.
https://doi.org/10.1093/molbev/msn083
Ribera, I. (2000) Biogeography and conservation of Iberian water beetles. Biologica Conservation, 92 (2), 131–150.
https://doi.org/10.1016/S0006-3207(99)00048-8
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180
Sharma, P. (2014) Morphological and molecular identification of three Ceriodaphnia species (Cladocera: Daphniidae) from Australia. Advances in Zoology, 2014, 25813.
https://doi.org/10.1155/2014/258134
Sharma, P. & Kotov, A.A. (2013) Molecular approach to identify sibling species of the Ceriodaphnia cornuta complex (Cladocera: Daphniidae) from Australia with notes on the continental endemism of this group. Zootaxa, 3702 (1), 79–89.
https://doi.org/10.11646/zootaxa.3702.1.5
Sharma, P., Elias-Gutierrez, M. & Kobayashi, T. (2014) Identification of common cladocerans and calanoids in two south Australian reservoirs using DNA barcoding and morphological analysis: an integrative approach. Crustaceana, 87 (7), 834–855.
https://doi.org/10.1163/15685403-00003333
Sinev, A.Y. & Lopez-Blanco, C. (2018) А new species of Alona Baird, 1843 (Cladocera: Chydoridae) from the ancient Lake Ohrid. Zootaxa, 4526 (4), 434–446.
https://doi.org/10.11646/zootaxa.4526.4.2
Sinev, A.Y., Alonso, M., Miracle, M.R. & Sahuquillo, M. (2012) The West Mediterranean Alona azorica Frenzel & Alonso, 1988 (Cladocera: Anomopoda: Chydoridae) is composed of two species. Zootaxa, 3276 (1), 51–68.
https://doi.org/10.11646/zootaxa.3276.1.3
Šrámek-Hušek, R., Strašcraba, M. & Brtek, J. (1962) Lupenonožci-Branchiopoda. Fauna ČSSR, Praha, 16, 1–472.
Taylor, D.J., Connelly, S.J. & Kotov, A.A. (2020) The Intercontinental phylogeography of neustonic daphniids. Scientific Reports, 10, 1–12.
https://doi.org/10.1038/s41598-020-58743-8
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W –improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.
https://doi.org/10.1093/nar/22.22.4673
deWaard, J.R., Sacherova, V., Cristescu, M.E., Remigio, E.A., Crease, T.J. & Hebert, P.D. (2006) Probing the relationships of the branchiopod crustaceans. Molecular Phylogenetics and Evolution, 39 (2), 491–502.
https://doi.org/10.1016/j.ympev.2005.11.003