The discovery and exploration of cryptic species have been profoundly expedited thanks to developments in molecular biology and phylogenetics. In this study, we apply a reverse taxonomy approach to the Brachionus calyciflorus species complex, a commonly studied freshwater monogonont rotifer. By combining phylogenetic, morphometric and morphological analyses, we confirm the existence of four cryptic species that have been recently suggested by a molecular study. Based on these results and according to an exhaustive review of the taxonomic literature, we name each of these four species and provide their taxonomic description alongside a diagnostic key.

Department of Zoology School of Biology Aristotle University of Thessaloniki Τhessaloniki Greece

Division of Genetics and Physiology Department of Biology University of Turku Turku Finland

Institute of Scientific Instruments Academy Of Sciences of the Czech Republic Brno Czech Republic

Netherlands Institute of Ecology Department of Aquatic Ecology Wageningen The Netherlands

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Hajibabaei M, Singer GAC, Hebert PDN, Hickey DA. DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends Genet. 2007; 23(4):167–72. 10.1016/j.tig.2007.02.001 PubMed DOI

Taylor HR, Harris WE. An emergent science on the brink of irrelevance: a review of the past 8 years of DNA barcoding. Mol Ecol Resour. 2012; 12(3):377–388. 10.1111/j.1755-0998.2012.03119.x PubMed DOI

Knowlton N. Sibling species in the sea. Annu Rev Ecol Evol Syst. 1993; 24(1):189–216.

Bickford D, Lohman DJ, Navjot SS, Ng PKL, Meier R, Winker K, et al. Cryptic species as a window on diversity and conservation. Trends Ecol Evol. 2007; 22: 148–155. 10.1016/j.tree.2006.11.004 PubMed DOI

Scheffers BR, Joppa LN, Pimm SL, Laurance WF. What we know and don’t know about Earth’s missing biodiversity. Trends Ecol Evol. 2012; 27(9):501–510. 10.1016/j.tree.2012.05.008 PubMed DOI

Padial JM, Miralles A, De la Riva I, Vences M. The integrative future of taxonomy. Front Zool. 2010; 7:16 10.1186/1742-9994-7-16 PubMed DOI PMC

Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian E, Crozier RH. Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol. 2010; 55:421–438. 10.1146/annurev-ento-112408-085432 PubMed DOI

Schlick-Steiner BC, Seifert B, Stauffer C, Christian E, Crozier RH. Without morphology, cryptic species stay in taxonomic crypsis following discovery. Trends Ecol Evol. 2007; 22(8): 391–392. 10.1016/j.tree.2007.05.004 PubMed DOI

Segers H, Smet WHD, Fischer C, Fontaneto D, Michaloudi E, Wallace RL, et al. Towards a list of available names in zoology, partim Phylum Rotifera. Zootaxa. 2012; 3179(1):61–68.

Cianferoni F, Bartolozzi L. Warning: potential problems for taxonomy on the horizon? Zootaxa. 2016; 4139(1):128–130. doi: 10.11646/zootaxa.4139.1.8 PubMed DOI

Santos CMD, Amorim DS, Klassa B, Fachin DA, Nihei SS, Carvalho CJB, et al. On typeless species and the perils of fast taxonomy. Syst Entomol. 2016; 41(3):511–515.

Declerck SAJ, Malo AR, Diehl S, Waasdorp D, Lemmen KD, Proios K, et al. Rapid adaptation of herbivore consumers to nutrient limitation: eco-evolutionary feedbacks to population demography and resource control. Ecol Lett. 2015; 18(6):553–562. 10.1111/ele.12436 PubMed DOI

Declerck SAJ, Papakostas S. Monogonont rotifers as model systems for the study of micro-evolutionary adaptation and its eco-evolutionary implications. Hydrobiologia. 2017; 796(1):131–144.

Markmann M, Tautz D. Reverse taxonomy: an approach towards determining the diversity of meiobenthic organisms based on ribosomal RNA signature sequences. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2005; 360(1462):1917–1924. 10.1098/rstb.2005.1723 PubMed DOI PMC

Pante E, Schoelinck C, Puillandre N. From Integrative Taxonomy to Species Description: One Step Beyond. Syst Biol. 2015; 64(1):152–60. 10.1093/sysbio/syu083 PubMed DOI

Wallace RL, Snell TW, Ricci C, Nogrady T. Rotifera. 1, biology, ecology and systematics. (2nd ed.). Ghent/Leiden: Kenobi Productions/ Backhuys Publishers; 2006

Gómez A, Serra M, Carvalho GR, Lunt DH. speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus Plicatilis (Rotifera). Evolution. 2002; 56(7):1431–1444. PubMed

Fontaneto D, Kaya M, Herniou EA, Barraclough TG. Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy. Mol Phylogenet Evol. 2009; 53(1):182–189. 10.1016/j.ympev.2009.04.011 PubMed DOI

Mills S, Alcántara-Rodríguez JA, Ciros-Pérez J, Gómez A, Hagiwara A, Galindo KH, et al. Mills S, Alcántara-Rodríguez JA, Ciros-Pérez J, Gómez A, Hagiwara A, Galindo KH, et al. Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy. Hydrobiologia. 2017; 796(1):39–58.

Papakostas S, Michaloudi E, Proios K, Brehm M, Verhage L, Rota J, et al. Integrative taxonomy recognizes evolutionary units despite widespread mitonuclear discordance: evidence from a rotifer cryptic species complex. Syst Biol. 2016; 65(3):508–524. 10.1093/sysbio/syw016 PubMed DOI

Fontaneto D. Molecular phylogenies as a tool to understand diversity in rotifers. Internat Rev Hydrobiol. 2014; 99(1–2):178–187.

Suatoni E, Vicario S, Rice S, Snell T, Caccone A. An analysis of species boundaries and biogeographic patterns in a cryptic species complex: The rotifer–Brachionus plicatilis. Mol Phylogenet Evol. 2006; 41(1):86–98. 10.1016/j.ympev.2006.04.025 PubMed DOI

Fontaneto D, Flot J-F, Tang CQ. Guidelines for DNA taxonomy, with a focus on the meiofauna. Mar Biodiv. 2015; 45(3):433–451.

Ciros-Pérez J, Gómez A, Serra M. On the taxonomy of three sympatric sibling species of the Brachionus plicatilis (Rotifera) complex from Spain, with the description of B. ibericus n. sp. J Plankton Res. 2001; 23(12):1311–1328.

Fontaneto D, Giordani I, Melone G, Serra M. Disentangling the morphological stasis in two rotifer species of the Brachionus plicatilis species complex. Hydrobiologia. 2007; 583(1):297–307.

Michaloudi E, Mills S, Papakostas S, Stelzer C-P, Triantafyllidis A, Kappas I, et al. Morphological and taxonomic demarcation of Brachionus asplanchnoidis Charin within the Brachionus plicatilis cryptic species complex (Rotifera, Monogononta). Hydrobiologia. 2017; 796(1):19–37.

Gilbert JJ. Competition between Rotifers and Daphnia. Ecology. 1985; 66(6):1943–1950.

Guo R, Snell TW, Yang J. Ecological strategy of rotifer Brachionus calyciflorus exposed to predator- and competitor-conditioned media. Hydrobiologia. 2011; 658(1):163–171.

Becks L, Agrawal AF. The Evolution of Sex Is Favoured During Adaptation to New Environments. PLoS Biol. 2012; 10(5):e1001317 10.1371/journal.pbio.1001317 PubMed DOI PMC

Scheuerl T, Stelzer C-P. Patterns and dynamics of rapid local adaptation and sex in varying habitat types in rotifers. Ecol Evol. 2013; 3(12):4253–4264. 10.1002/ece3.781 PubMed DOI PMC

Snell TW, Moffat BD. A 2-d Life cycle test with the rotifer Brachionus calyciflorus. Environ Toxicol Chem. 1992; 11(9):1249–1257.

Cruciani V, Iovine C, Thomé J-P, Joaquim-Justo C. Impact of three phthalate esters on the sexual reproduction of the Monogonont rotifer, Brachionus calyciflorus. Ecotoxicology. 2016; 25(1):192–200. 10.1007/s10646-015-1579-5 PubMed DOI

Han J, Kim D-H, Kim H-S, Kim H-J, Declerck SAJ, Hagiwara A, et al. Genome-wide identification of 31 cytochrome P450 (CYP) genes in the freshwater rotifer Brachionus calyciflorus and analysis of their benzo[α]pyrene-induced expression patterns. Comp Biochem Physiol Part D Genomics Proteomics. 2018; 25:26–33. 10.1016/j.cbd.2017.10.003 PubMed DOI

Lim LC, Wong CC. Use of the rotifer, Brachionus calyciflorus Pallas, in freshwater ornamental fish larviculture. Hydrobiologia. 1997; 358(1–3):269–273.

Shiri Harzevili A, De Charleroy D, Auwerx J, Vught I, Van Slycken J, Dhert P, et al. Larval rearing of burbot (Lota lota L.) using Brachionus calyciflorus rotifer as starter food. J Appl Ichthyol. 2003; 19(2):84–7.

Kim H-S, Lee B-Y, Han J, Jeong C-B, Hwang D-S, Lee M-C, et al. The genome of the freshwater monogonont rotifer Brachionus calyciflorus. Mol Ecol Resour. 2018; 18:646–655. 10.1111/1755-0998.12768 PubMed DOI

Ahlstrom EH. A revision of the rotatorian genera Brachionus and Platyias with descriptions of one new species and two new varieties. Bulletin of the American Museum of Natural History. 1940; 77:143–184.

Koste W. Rotatoria, die Rãdertiere Mitteleuropas. Berlin: Gebrüder Borntraeger; 1978.

Kutikova LA, Fernando CH. Brachionus calyciflorus Pallas (Rotatoria) in Inland Waters of Tropical Latitudes. Int Revue ges Hydrobiol Hydrogr. 1995; 80(3):429–41.

Segers H. Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa. 2007; 1564: 1–104.

Gilbert JJ, Walsh EJ. Brachionus calyciflorus is a species complex: mating behavior and genetic differentiation among four geographically isolated strains. Hydrobiologia. 2005; 546(1):257–65.

Xiang X, Xi Y, Wen X, Zhang G, Wang J, Hu K. Patterns and processes in the genetic differentiation of the Brachionus calyciflorus complex, a passively dispersing freshwater zooplankton. Mol Phylogenet Evol. 2011; 59(2):386–98. 10.1016/j.ympev.2011.02.011 PubMed DOI

Gomez A, Carvalho GR. Sex, parthenogenesis and genetic structure of rotifers: microsatellite analysis of contemporary and resting egg bank populations. Mol Ecol. 2000; 9:203–214. PubMed

Will S, Joshi T, Hofacker IL, Stadler PF, Backofen R. LocARNAP: Accurate boundary prediction and improved detection of structural RNAs. RNA. 2012; 18:900–914. 10.1261/rna.029041.111 PubMed DOI PMC

Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009; 25:1451–1452. 10.1093/bioinformatics/btp187 PubMed DOI

Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, et al. Sequencebased species delimitation for the DNA taxonomy of undescribed insects. Syst Biol. 2006; 55:595–609. PubMed

Abramoff MD, Magalhaes PJ, Ram SJ. Image processing with ImageJ. Biophotonics International. 2004; 11:36–42.

Fu Y, Hirayama K, Natsukari Y. Morphological differences between two types of the rotifer Brachionus plicatilis O.F. Mόller J. Exp. Mar. Biol. Ecol. 1991; 151:29–41.

Proios K, Michaloudi E, Papakostas S, Kappas I, Vasileiadou K, Abatzopoulos TJ. Updating the description and taxonomic status of Brachionus sessilis Varga, 1951 (Rotifera: Brachionidae) based on detailed morphological analysis and molecular data. Zootaxa. 2014; 3873:345–370. doi: 10.11646/zootaxa.3873.4.2 PubMed DOI

International Commission on Zoological Nomenclature [Cited 2018 June]. Available from http://iczn.org/lan/rotifer, PubMed PMC

Jersabek CD, Leitner MF. The Rotifer World Catalog. World Wide Web electronic publication; 2013. [Cited 2017 December]. Available from http://www.rotifera.hausdernatur.at/

Neděla V, Tihlaříková E, Runštuk J, Hudec J. High-efficiency detector of secondary and backscattered electrons for low-dose imaging in the ESEM, Ultramicroscopy. 2018; 184:1–11. PubMed

Neděla V, Tihlaříková E, Hřib J. The Low-Temperature Method for Study of Coniferous Tissues in the Environmental Scanning Electron Microscope. Microscopy Research Technique. 2015; 78:13–21. 10.1002/jemt.22439 PubMed DOI

Đorđević B, Neděla V, Tihlaříková E, Trojan V, Havel V. Effects of copper and arsenic stress on the development of Norway spruce somatic embryos and their visualization with the environmental scanning electron microscope. 2018; 10.1016/j.nbt.2018.05.005 PubMed DOI

De Smet WH. Preparation of rotifer trophi for light and scanning electron microscopy. Hydrobiologia. 1998; 387/388:117–121

Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, et al. 2015. Vegan: Community Ecology Package. R package version 2.3–2. Vienna, Austria: R Foundation for Statistical Computing; Available from: URL http://CRAN.R-project.org/package=vegan

IBM Corp. Released 2012. IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp.

Pallas PS. Elenchus zoophytorum, sistens generum adumbrationes generaliores et specierum cognitarum succintas descriptiones: cum selectis auctorum synonymis. Frankfort: Hagae-comitum; 1766.

Ehrenberg CG. Organisation, Systematik und geographisches Verhältnis der Infusionsthierchen Zwei Vorträge in der Akademie der Wissenschaften zu Berlin gehalten in den Jahren 1828 [Die geographische Verbreitung der Infusionsthierchen in Nord-Afrika und West-Asien, beobachtet auf Hemprich und Ehrenbergs Reisen] und 1830 [Beiträge zur Kenntnis der Organisation der Infusorien und ihrer geographischen Verbreitung, besonders in Sibirien]. Berlin: Druckerei der königlichen Akademie der Wissenschaften; 1830.

Ehrenberg CG. Die Infusionsthierchen als vollkommene Organismen Ein Blick in das tiefere organische Leben der Natur. Leipzig: Verlag von Leopold Voss; 1838.

Weisse JF. Beschreibung einiger neuer Infusorien, welche in stehenden Wässern bei St. Petersburg vorkommen. Bulletin de la Classe Physico-Mathématique de l'Académie Impériale des Sciences de St.-Pétersbourg. 1845; 4:138–143.

Schmarda LK. Zur Naturgeschichte Ägyptens. Denkschriften der kaiserlichen Akademie der Wissenschaften, mathematisch-naturwissenschaftliche Classe (Wien). 1854; 7/2:1–28.

Daday E. Neue Beiträge zur Kenntnis der Rädertiere. Mathematische und Naturwissenschaftliche Berichte aus Ungarn. 1883; 1:261–264.

Plate L. Beiträge zur Naturgeschichte der Rotatorien. Jenaische Zeitschrift für Naturwissenschaft. 1886; 19:1–120.

France RH. Beiträge zur Kenntnis der Rotatorienfauna Budapest's. Természetrajzi Füzetek kiadja a Magyar nemzeti Múzeum. 1894; 17:166–184.

Brehm V. Über die Mikrofauna chinesischer und südasiatischer Süsswasserbecken. Arch Hydrobiol. 1909; 4:207–224.

Spandl H. Brachionus pala Ehrbg. var. mucronatus nov. var. Zool Anz.1922; 54: 275.

Jersabek CD, Bolortsetseg E. Mongolian rotifers (Rotifera, Monogononta)–a checklist with annotations on global distribution and autecology. Proceeding of the Academy of Natural Sciences of Philadephia 2010; 159:119–168.

Segers H, Murugan G, Dumont HJ. On the taxonomy of the Brachionidae: description of Plationus n. gen. (Rotifera, Monogononta). Hydrobiologia. 1993; 268(1):1–8.

Gosse PH. A catalogue of Rotifera found in Britain; with descriptions of five new genera and thirty-two new species. Annals and Magazine of Natural History. 1851; 8:197–203.

Wierzejski A. Liste de rotifères observes en Galicie (Autriche-Hongrie). Bulletin de la Société zoologique de France. 1891; 16:49–52.

Koste W, Shiel RJ. Rotifera from Australian inland waters. II. Epiphanidae and Brachionidae (Rotifera: Monogononta). Invert Systematics. 1987; 1(7):949–1021.

Gilbert JJ, Waage JK. Asplanchna, Asplanchna-substance, and posterolateral spine length variation of the rotifer Brachionus calyciflorus in a natural environment. Ecology. 1967; 48(6):1027–31.

Gilbert JJ. Further observations on developmental polymorphism and its evolution in the rotifer Brachionus calyciflorus. Freshw Biol. 1980; 10(3):281–94.

Stemberger RS. Food limitation. spination, and reproduction in Brachionus calyciflorus. Limnol Oceanogr. 1990; 35(1):33–44.

Gilbert JJ. Spine development in two taxa of Brachionus calyciflorus from Lake Littra, Australia: constitutive and induced defenses against Asplanchna. J Plankton Res. 2017; 39(6):962–71.

Papakostas S, Michaloudi E, Triantafyllidis A, Kappas I, Abatzopoulos TJ. Allochronic divergence and clonal succession: two microevolutionary processes sculpturing population structure of Brachionus rotifers. Hydrobiologia. 2013; 700(1):33–45.

Revalidation of Mazama rufa (Illiger 1815) (Artiodactyla: Cervidae) as a Distinct Species out of the Complex Mazama americana (Erxleben 1777)

In-situ preparation of plant samples in ESEM for energy dispersive x-ray microanalysis and repetitive observation in SEM and ESEM

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