Skip to main content Skip to main navigation menu Skip to site footer
Article
Published: 2020-07-13

A proposal for a new generic structure of the killifish family Aphaniidae, with the description of Aphaniops teimorii (Teleostei: Cyprinodontiformes)

Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, 10115 Berlin, Germany.
Hacettepe University, Faculty of Science, Biology Department, Beytepe Campus, 06800 Ankara, Turkey.
Pisces freshwater fish taxonomy biodiversity generic concepts

Abstract

Following an exhaustive review of published molecular data and morphological characters, we propose a new generic classification for the Cyprinodontiform family Aphaniidae. The generic concept applied is based on monophyly, reasonable compactness, and morphological diagnoses. The proposed genera are monophyletic and compact groups that can be diagnosed by a combination of morphological characters. All species in Aphaniidae are morphologically homogeneous and have similar scale patterns, fin positions, and meristic characters. However, only a handful of morphological characters, including colour patterns, permit identification. We propose separation of Aphaniidae into eight monophyletic genera: Anatolichthys, Aphaniops, Aphanius, Kosswigichthys, Paraphanius, and Tellia, in addition to the new genera Esmaeilius and Apricaphanius, which are described for the species of the A. sophiae and A. iberus species groups, respectively. The original description of Aphanius hormuzensis does not fulfil the criteria of the International Commission on Zoological Nomenclature, therefore this taxon is re-described as A. teimorii. Esmaeilius arakensis, E. kavirensis, E. mesopotamicus, and E. pluristriatus are treated as synonyms of E. sophiae. Esmaeilius farsicus is a junior synonym of E. persicus (Jenkins, 1910). The fossil genus Brachylebias is considered as incertae sedis since it lacks diagnostic characters which would permit it to be assigned to any of the extant genera recognised in this study.

 

References

  1. Akşıray, F. (1948) Türkiye Cyprinodontidleri hakkında I. Türkische Cyprinodontiden I. Revue de la Faculté des Sciences de I’Université d’Istanbul, 13, 97–142.

    Annabi, A. Said, K. & Reichenbacher, B. (2013) Inter-population differences in otolith morphology are genetically encoded in the killifish Aphanius fasciatus (Cyprinodontiformes). Scientia Marina, 77 (2), 269–279.

    https://doi.org/10.3989/scimar.03763.02A

    Avise, C.J. & Liu, J. (2011) On the temporal inconsistencies of Linnean taxonomic ranks. Biological Journal of the Linnean Society, 102 (4), 707–714.

    https://doi.org/10.1111/j.1095-8312.2011.01624.x

    Blanco, J.L., Hrbek, T. & Doadrio, I. (2006) A new species of the genus Aphanius (Nardo, 1832) (Actinopterygii, Cyprinodontidae) from Algeria. Zootaxa, 1158 (1), 39–53.

    https://doi.org/10.11646/zootaxa.1158.1.2

    Bodenheimer, F.S. (1935) Animal life in Palestine. L. Mayer, Jerusalem, 507 pp.

    Borkenhagen, K. (2017) Taxonomy, phylogeny and zoogeography of the hexaploid Torini of the Middle East and North Africa. Dissertation, Johann Wolfgang Goethe-Universität in Frankfurt am Main, 1466 pp. [http://publikationen.ub.uni-frankfurt.de/files/45041/Dissertation_Borkenhagen_ohne_CV.pdf]

    Bragança, P.H.N. & Costa, W.J.E.M. (2019) Multigene fossil-calibrated analysis of the African lampeyes (Cyprinodontoidei: Procatopodidae) reveals an early Oligocene origin and Neogene diversification driven by palaeogeographic and palaeoclimatic events. Organisms Diversity & Evolution, 19, 303–320.

    https://doi.org/10.1007/s13127-019-00396-1

    Cavraro, F., Malavasi, S., Torricelli, P., Gkenas, C., Liousia, V., Leonardos, I., Kappas, I., Abatzopoulos, T.J. & Triantafyllidis, A. (2017) Genetic structure of the South European toothcarp Aphanius fasciatus (Actinopterygii: Cyprinodontidae) populations in the Mediterranean basin with a focus on the Venice lagoon, The European Zoological Journal, 84 (1), 153–166.

    https://doi.org/10.1080/24750263.2017.1290154

    Costa, W.J.E.M. (2012a) Oligocene killifishes (Teleostei: Cyprinodontiformes) from southern France: relationships, taxonomic position, and evidence of internal fertilization. Vertebrate Zoology, 62 (3), 371–386.

    Costa, W.J.E.M. (2012b). The caudal skeleton of extant and fossil cyprinodontiform fishes (Teleostei: Atherinomorpha): comparative morphology and delimitation of phylogenetic characters. Vertebrate Zoology, 62 (2), 161–180.

    Doadrio, I. Carmona, J.A. & Fernandez-Delgado, C. (2002) Morphometric study of the Iberian Aphanius (Actinopterygii: Cyprinodontiformes), with description of a new species. Folia Zoologica, 51, 67–79.

    Erk’akan, F. & Özdemir, F. (2011) Revision of the fish fauna of Seyhan and Ceyhan River basins in Turkey. Research Journal of Biological Sciences, 6, 1–8.

    https://doi.org/10.3923/rjbsci.2011.1.8

    Ermin, R. (1946) Cyprinodontid’lerde pul reduksiyonu. Schuppenreduktion bei Zahnkarpfen (Cyprinodontidae). Revue de la Faculté des Sciences de I’Université d’Istanbul, Series B, 10, 244–250.

    Esmaeili, H.R., Teimori, A., Gholami, Z., Zarei, N. & Reichenbacher, B. (2012) Re-validation and re-description of an endemic and endangered species, Aphanius pluristriatus (Jenkins, 1910) (Teleostei, Cyprinodontidae), from southern Iran. Zootaxa, 3208 (1), 58–67.

    https://doi.org/10.11646/zootaxa.3208.1.4

    Esmaeili, H.R., Teimori, A., Sayyadzadeh, G., Masoudi, M. & Reichenbacher, B. (2014a) Phylogenetic relationships of the tooth-carp Aphanius (Teleostei: Cyprinodontidae) in the river systems of southern and south-western Iran based on mtDNA sequences. Zoology in the Middle East, 60 (1), 29–38.

    https://doi.org/10.1080/09397140.2014.892329

    Esmaeili, H.R., Teimori, A., Gholami, Z. & Reichenbacher, B. (2014b) Two new species of the tooth-carp Aphanius (Teleostei: Cyprinodontidae) and the evolutionary history of the Iranian inland and inland-related Aphanius species. Zootaxa, 3786 (3), 246–268.

    https://doi.org/10.11646/zootaxa.3786.3.2

    Esmaeili, H.R., Teimori, A., Zarei, F. & Gholami, S. (2020) DNA barcoding and species delimitation of the Old World tooth-carps, family Aphaniidae Hoedeman, 1949 (Teleostei: Cyprinodontiformes). PLoS ONE, 15(4), e0231717.

    https://doi.org/10.1371/journal.pone.0231717

    Freyhof, J., Kaya, C., Turan, D. & Geiger, M. (2019) Review of the Oxynoemacheilus tigris group with the description of two new species from the Euphrates drainage (Teleostei: Nemacheilidae). Zootaxa, 4612 (1), 29–57.

    https://doi.org/10.11646/zootaxa.4612.1.2

    Freyhof, J., Özuluǧ, M. & Saç, G. (2017) Neotype designation of Aphanius iconii, first reviser action to stabilise the usage of A. fontinalis and A. meridionalis and comments on the family group names of fishes placed in Cyprinodontidae (Teleostei: Cyprinodontiformes). Zootaxa, 4294 (5), 573–585.

    https://doi.org/10.11646/zootaxa.4294.5.6

    Freyhof, J., Kaya, C., Bayçelebi, E., Geiger, M. & Turan D. (2018) Generic assignment of Leuciscus kurui Bogutskaya from the upper Tigris drainage, and a replacement name for Alburnus kurui Mangit & Yerli (Teleostei: Leuciscidae). Zootaxa, 4410 (1), 113–135.

    https://doi.org/10.11646/zootaxa.4410.1.6

    Gaudant, J. (1978) Sur une nouvelle espèce de Poissons Téléostéens Cyprinodontiformes de l’Oligocène des environs de Manosque (Alpes-de-Haute-Provence). Géologie Méditerranéenne, 5, 281–290.

    Gaudant, J. (2011) Aphanius persicus (Priem, 1908) (Pisces, Teleostei, Cyprinodontidae): une nouvelle combinaison pour Brachylebias persicus Priem, 1908, du Miocène supérieur des environs de Tabriz (Iran). Geodiversitas, 33, 347–356.

    https://doi.org/10.5252/g2011n2a9

    Gaudant, J, (2013) Occurrence of poeciliid fishes (Teleostei, Cyprinodontiformes) in the European Oligo-Miocene: the genus Paralebias nov. gen. Neues Jahrbuch für Geologie und Paläontologie Stuttgart. Abhandlungen, 267/2, 215–222.

    https://doi.org/10.1127/0077-7749/2013/0305

    Geiger, M.F., Herder, F., Monaghan, M.T., Almada, V., Barbieri, R., Bariche, M., Berrebi, P., Bohlen, J., Casal-Lopez, M., Delmastro, G.B., Denys, G.P.J., Dettai, A., Doadrio, I., Kalogianni, E., Kärst, H., Kottelat, M., Kovačić, M., Laporte, M., Lorenzoni, M., Marčić, Z., Özuluğ, M., Perdices, A., Perea, S., Persat, H., Porcelotti, S., Puzzi, C., Robalo, J., Šanda, R., Schneider, M., Šlechtová, V., Stoumboudi, M., Walter, S. & Freyhof, J. (2014) Spatial heterogeneity in the Mediterranean Biodiversity Hotspot affects barcoding accuracy of its freshwater fishes. Molecular Ecology Resources, 14, 1210–1221.

    https://doi.org/10.1111/1755-0998.12257

    Getahun, A. & Lazara, K.J. (2001) Lebias stiassnyae: a new species of killifish from Lake Afdera, Ethiopia (Teleostei: Cyprinodontidae). Copeia, 1, 150–153.

    https://doi.org/10.1643/0045-8511(2001)001[0150:LSANSO]2.0.CO;2

    Gholami, Z., Esmaeili, H.R., Erpenbeck, D. & Reichenbacher, B. (2014) Phylogenetic analysis of Aphanius from the endorheic Kor River basin in the Zagros Mountains, southwestern Iran (Teleostei: Cyprinodontiformes: Cyprinodontidae). Journal of Zoological Systematics and Evolutionary Research, 52, 130–141.

    https://doi.org/10.1111/jzs.12052

    Gholami, Z., Teimori A., Esmaeili, H.R., Schulz-Mirbach, T. & Reichenbacher, B. (2013) Scale surface microstructure and scale size in the tooth-carp genus Aphanius (Teleostei, Cyprinodontidae) from endorheic basins in Southwest Iran. Zootaxa, 3619 (4), 467–490.

    https://doi.org/10.11646/zootaxa.3619.4.5

    Gonzales, E.G., Pedraza-Lara, C. & Doadrio, I. (2014) Genetic diversity and population history of the endangered killifish Aphanius baeticus. Journal of Heredity, 105, 597–610.

    https://doi.org/10.1093/jhered/esu034

    Goren, M. (1974) The freshwater fishes of Israel. Israel Journal of Zoology, 23, 67–118.

    https://doi.org/10.1080/00212210.1974.10688400

    Grimm, H. (1980) Investigations on the problem of scale reduction and sulphate tolerance of West-Anatolian Cyprinodonts (Pisces). Internationaler Revue der Gesellschaft für Hydrobiologie, 65, 517–533.

    Hennig, W. (1966) Phylogenetic systematics. University of Illinois Press, Urbana, Illinois, 263 pp.

    Hoedeman, J.J. (1951) Rediagnosis of the old world cyprinodont genus Aphanius. Beaufortia, 1 (1), 1–6.

    Hrbek, T. & Meyer, A. (2003) Closing of the Tethys Sea and the phylogeny of Eurasian killifishes (Cyprinodontiformes: Cyprinodontidae). Journal of Evolutionary Biology, 16, 7–26.

    https://doi.org/10.1046/j.1420-9101.2003.00475.x

    Hrbek, T., Küçük, F., Frickey, T., Stölting, K.N., Wildekamp, R.H. & Meyer, A. (2002) Molecular phylogeny and historical biogeography of the Aphanius (Pisces, Cyprinodontiformes) species complex of central Anatolia, Turkey. Molecular Phylogenetics and Evolution, 25, 125–137.

    https://doi.org/10.18864/iujfas.3778

    ICZN [International Code of Zoological Nomenclature] (1999) International Code of Zoological Nomenclature. 4th Edition. International Trust for Zoological Nomeclature, London, 306 pp.

    Johns, G.C. & Avise, J.C. (1998) A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Molecular Biology and Evolution, 15, 1481–1490.

    https://doi.org/10.1093/oxfordjournals.molbev.a025875

    Kaiser, H., Crother, B.A., Kelly, C.M.R., Luiselli, L., O’Shea, M., Ota, H., Passos, P., Schleip, W.D. & Wüster, W. (2013) Best practices: In the 21st century, taxonomic decisions in herpetology are acceptable only when supported by a body of evidence and published via peer-review. Herpetological Review, 2013, 44, 8–23.

    Kara, C., Alp, A. & Şimşekli, M. (2010) Distribution of fish fauna on the upper and middle basin of Ceyhan River, Turkey. Turkish Journal of Fisheries and Aquatic Sciences, 10, 111–122.

    https://doi.org/10.4194/trjfas.2010.0116

    Kosswig, C. & Sözer, F. (1945) Nouveaux Cyprinodontides de l’Anatolie centrale. Revue de la Faculté des Sciences de l‘Université d‘Instanbul, Série B (Sciences Naturelles), 10, 77–83.

    Kottelat, M. (1997) European freshwater fishes. An heuristic checklist of the freshwater fishes of Europe (exclusive of former USSR), with an introduction for non-systematists and comments on nomenclature and conservation. Biologia, Bratislava, Section Zoology, 52 (Supplement 5), 1–271

    Kottelat, M. (2012) Conspectus cobitidum: An inventory of the loaches of the world (Teleostei Cypriniformes Cobitoidei). The Raffles Bulletin of Zoology, Supplement 26, 1–199.

    Kottelat, M., Barbieri, R. & Stoumboudi, M. (2007) Aphanius almiriensis, a new species of toothcarp from Greece (Teleostei: Cyprinodontidae). Revue Suisse de Zoologie, 114, 13–31.

    https://doi.org/10.5962/bhl.part.80385

    Kottelat, M. & Freyhof, J. (2007) Handbook of European freshwater fishes. Kottelat, Cornol and Freyhof, Berlin, xiv + 646 pp.

    Krupp, F., (1985) Systematik und Zoogeographie der Süsswasserfische des levantinischen Grabenbruchsystems und der Ostküste des Mittelmeers. Dissertation, Johannes Gutenberg Universität, Mainz, 215 pp.

    McMahan, C.D., Matamoros, W.A., Piller, K.R. & Chakrabarty, P. (2015) Taxonomy and systematics of the herichthyins (Cichlidae: Tribe Heroini), with the description of eight new Middle American genera. Zootaxa, 3999 (2), 211–234.

    https://doi.org/10.11646/zootaxa.3999.2.3

    Meri, S. & Mace, G.M. (2007) New taxonomy and the origin of species. Plos Biology, 5 (7), e194.

    https://doi.org/10.1371/journal.pbio.0050194

    Mohammadian-Kalat, T., Esmaeili, H.R., Aliabadian, M. & Freyhof, F. (2017) Re-description of Alburnus doriae, with comments on the taxonomic status of A. amirkabiri, A. mossulensis, A. sellal and Petroleuciscus esfahani (Teleostei: Cyprinidae). Zootaxa, 4323 (4), 487–502.

    https://doi.org/10.11646/zootaxa.4323.4.3

    Parenti, L.R. (1981) A phylogenetic and biogeographic analysis of cyprinodontiform fishes (Teleostei, Atherinomorpha). Bulletin of the American Museum of Natural History, 168, 335–557.

    Pellegrin, J. (1911) Poissons de Syrie recueillis par M. Henri Gadeau der Kerville. Bulletin de la Société Zoologique de France, 36, 107–111.

    Pellegrin, J. (1921) Le poissons des eaux douces de l’Afrique du Nord Francaise, Maroc, Tunisie, Sahara. Mémoires de la Société des Sciences naturelles du Maroc, 1 (2), 1–216, 96 figs.

    Pellegrin, J. (1923) Etude sur les poissons rapportes par M. Henri Gadeau de Kerville de son vovyage zoologique en Syrie. In: H. Gadeau de Kerville, Voyage zoologique d‘ Henri Gadeau de Kerville en Syrie (Avril–Juin 1908), 4, pp. 5–37.

    Priem, F. (1908) Poissons fossiles de Perse (Mission de Morgan). In: Annales Publiees Sous la Direction de J. Morgan, Delegation scientifique en Perse. Annales d’Histoire naturelle, Paris, 1, 1–25.

    Reichenbacher, B. & Gaudant, J. (2003) On Prolebias meyeri (Agassiz) (Teleostei, Cyprinodontiformes) from the Oligo-Miocene of the Upper Rhinegraben area, with the establishment of a new genus and a new species. Eclogae Geologica Helvetiae, 96, 509–520.

    Reichenbacher, B. & Kowalke, T. (2009) Neogene and present-day zoogeography of killifishes (Aphanius and Aphanolebias) in the Mediterranean and Paratethys areas. Palaeogeography, Palaeoclimatology, Palaeoecology, 281, 43–56.

    https://doi.org/10.1016/j.palaeo.2009.07.008

    Reichenbacher, B., Feulner, G.R. & Schulz-Mirbach, T. (2009a) Geographic variation in otolith morphology among freshwater populations of Aphanius dispar (Teleostei, Cyprinodontiformes) from the southeastern Arabian Peninsula. Journal of Morphology, 270, 469–484.

    https://doi.org/10.1002/jmor.10702

    Reichenbacher, B., Kamrani, E., Esmaeili, H.R. & Teimori, A. (2009b) The endangered cyprinodont Aphanius ginaonis (Holly, 1929) from southern Iran is a valid species: evidence from otolith morphology. Environmental Biology of Fishes, 86, 507–521.

    Říčan, O., Piálek, L., Dragová, K. & Novák, J. (2016) Diversity and evolution of the Middle American cichlid fishes (Teleostei: Cichlidae) with revised classification. Vertebrate Zoology, 66, 1–102.

    Robalo, J.I., Almada, V.C., Levi, A. & 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.

    https://doi.org/10.1016/j.ympev.2006.07.003

    Schulz-Mirbach, T., Reichenbacher, B., Yıldırım. Z. & Atalay, M.A. (2006) Otolith characteristics of species, subspecies, and populations of Aphanius Nardo, 1827 (Teleostei, Cyprinodontiformes) from Anatolia (Turkey). Journal of Natural History, 40, 27–28.

    https://doi.org/10.1080/00222930600964498

    Tan, M. & Armbruster, J.W. (2018) Phylogenetic classification of extant genera of fishes of the order Cypriniformes (Teleostei: Ostariophysi). Zootaxa, 4476 (1), 6–39.

    https://doi.org/10.11646/zootaxa.4476.1.4

    Teimori, A., Esmaeili, H.R. Erpenbeck, D. & Reichenbacher, B. (2014) A new and unique species of the genus Aphanius (Teleostei: Cyprinodontidae) from Southern Iran: A case of regressive evolution. Zoologischer Anzeiger, 253, 327–337.

    https://doi.org/10.1016/j.jcz.2013.12.001

    Teimori, A., Esmaeili, H.R., Gholami, Z., Zarei, N. & Reichenbacher, B. (2012) Aphanius arakensis, a new species of tooth-carp (Actinopterygii, Cyprinodontidae) from the endorheic Namak Lake basin in Iran. Zookeys, 215, 55–76.

    https://doi.org/10.3897/zookeys.215.1731

    Teimori, A., Esmaeili, H.R., Hamidan, N. & Reichenbacher, B. (2018a) Systematics and historical biogeography of the Aphanius dispar species group (Teleostei: Aphaniidae) and description of a new species from Southern Iran. Journal of Zoological Systematics and Evolutionary Research, 56, 579–598.

    https://doi.org/10.1111/jzs.12228

    Teimori, A., Motamedi, M. & Iranmanesh, A. (2018b) Comparative morphology of urohyal bone in brackish water species of the genus Aphanius Nardo, 1827 in the Persian Gulf and Southeastern Mediterranean Sea basins (Teleostei: Aphaniidae). Mediterranean Marine Science, 19 (2), 356–365.

    https://doi.org/10.12681/mms.15929

    Tortonese, E. (1938) Viaggio del dott. Enrico Festa in Palestina e in Siria (1893). Pesci. Bollettino dei Musei di Zoologia ed Anatomia Comparata della R. Università di Torino, Series 3, 46 (85), 313–358, pls. 1–2.

    Valdesalici, S., Brahimi, A. & Freyhof, J. (2019) First record of Aphanius almiriensis from Italy and notes on the distribution of Aphanius fasciatus (Teleostei: Aphaniidae). Journal of Applied Ichthyology, 35, 541–550.

    https://doi.org/10.1111/jai.13873

    Van Der Zee, J.R. & Vonk, R. (1991) Fisch Expeditionen in der Mahgreb. Die Aquarien und Terrarien Zeitschrift, 44, 255–257.

    Vasilyan, D., Reichenbacher, B. & Carnevale, G. (2009) A new fossil Aphanius species from the Upper Miocene of Armenia (Eastern Paratethys). Paläontologische Zeitschrift, 83, 511–519.

    https://doi.org/10.1007/s12542-009-0034-4

    Villwock, W. (1963) Genetische Analyse des Merkmals “Beschuppung” bei Anatolischen Zahnkarpfen (Pisces: Cyprinodontidae) im Auflöserversuch. Zoologischer Anzeiger, 170, 23–45.

    Villwock, W., Scholl, A. & Krupp, F. (1983) Zur Taxonomie, Verbreitung und Speziation des Formenkreises Aphanius dispar (Rüppell, 1828) und Beschreibung von Aphanius sirhani n. sp. (Pisces: Cyprinodontidae). Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut, 80, 251–277.

    Wildekamp, R.H. (1993) A world of killies. Atlas of the oviparous cyprinodontiform fishes of the world. The genera Adamas, Adinia, Aphanius, Aphyoplatys and Aphyosemion. American Killifish Association, Indiana, 311 pp.

    Wildekamp, R.H., Küçük, F., Ünlüsayin, M. & Neer, W.V. (1999) Species and subspecies of the genus Aphanius Nardo 1897 (Pisces: Cyprinodontidae) in Turkey. Turkish Journal of Zoology, 23, 23–44.

    Wiley, E.O. (1979) An annotated Linnaean Hierarchy, with comments on natural taxa and competing systems. Systematic Biology, 28 (3), 308–337.

    https://doi.org/10.1093/sysbio/28.3.308

    Yoğurtçuoğlu, B. & Ekmekçi, F.G. (2017) New records of Kızılırmak Toothcarp, Aphanius marassantensis from Central Yeşilırmak River Basin (Turkey) Turkish Journal of Fisheries and Aquatic Sciences, 17, 205–208.

    https://doi.org/10.4194/1303-2712-v17_1_22

    Yoğurtçuoğlu, B. & Freyhof, J. (2018) Aphanius irregularis, a new killifish from south western Anatolia (Cyprinodontiformes: Aphaniidae). Zootaxa, 4410 (2), 319–330.

    https://doi.org/10.11646/zootaxa.4410.2.4

    Yoğurtçuoğlu, B. & Freyhof, J. (2020) Fish occurrence database of the family Aphaniidae. Freshwater Metadata Journal, 48, 1–5.

    https://doi.org/10.15504/fmj.2020.48