Agrafia Szarowska et Falniowski, 2011 (Caenogastropoda: Hydrobiidae) in the Caucasus

Jozef Grego

Department of Comparative Anatomy, Institute of Zoology, Jagiellonian University, Cracow, Poland

Sebastian Hofman

Institute of Zoology Ilia State University, Tbilisi, Georgia

Levan Mumladze

Department of Malacology, Institute of Zoology, Jagiellonian University, Cracow, Poland

Andrzej Falniowski, e-mail:

Department of Malacology, Institute of Zoology, Jagiellonian University, Cracow, Poland

Freshwater gastropods of the Caucasus are poorly known. A few minute Belgrandiella-like gastropods were found in three springs in Georgia. Molecular markers: mitochondrial cytochrome oxidase subunit I (COI) and nuclear histone (H3) were used to infer their phylogenetic relationships. The phylogenetic trees placed them most closely to Agrafia from continental Greece. The p-distances indicated that two species occurred in the three localities. Two specimens from Andros Island (Greece) were also assigned to the genus Agrafia. The p-distances between the four taxa, most probably each representing a distinct species, were within the range of 0.026–0.043 for H3, and 0.089–0.118 for COI.

Key words
spring snail; DNA; Georgia; Andros; phylogeny

Barjadze Sh., Murvanidze M., Arabuli T., Mumladze L., Pkhakadze V., Djanashvili R., Salakaia M. 2015. Annotated list of invertebrates of the Georgian karst caves. Georgian Academic Book, Tbilisi.
Beran L., Hofman S., Falniowski A. 2015. Tanousia zrmanjae (Brusina, 1866) (Caenogastropoda: Truncatelloidea: Hydrobiidae): a living fossil. Folia Malacol. 23: 263–271.
Beran L., Osikowski A., Hofman S., Falniowski A. 2016. Islamia zermanica (Radoman, 1973) (Caenogastropoda: Hydrobiidae): morphological and molecular distinctness. Folia Malacol. 24: 25–30.
Bodon M. 1988. Note anatomiche su «Belgrandiella» hartwigschuetti Reischütz e revisione della sua posizione sistematica (Gastropoda: Prosobranchia: Hydrobiidae). Arch. Molluskenkd. 110: 55–63.
Boeters H. D. 1970. Die Gattung Microna Clessin, 1980 (Prosobranchia, Hydrobiidae). Arch. Molluskenkd. 100: 113–145.
Boeters H. D. 1998. Mollusca: Gastropoda: Superfamilie Rissooidea. In: Brauer A., Schwoerbel J., Zwick P. (eds). Süsswasserfauna von Mitteleuropa. Begründet von A. Brauer, 5/1–2. Gustav Fischer Verlag, Jena – Lübeck – Ulm.
Chertoprud E. S., Palatov D. M., Borisov R. R., Marinskiy V. V., Bizin M. S., Dbar R. S. 2016. Distribution and a comparative analysis of the aquatic invertebrate fauna in caves of the western Caucasus. Subterr. Biol. 18: 49–70.
Davis G. M., Wilke T., Spolsky C., Qiu C.-P., Qiu D.-C., Xia M.-Y., Zhang Y., Rosenberg G. 1998. Cytochrome oxidase I-based phylogenetic relationships among the Pomatiopsidae, Hydrobiidae, Rissoidae and Truncatelidae (Gastropoda: Caenogastropoda: Rissoacea). Malacologia 40: 251–266.
Edgar R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792–1797.
Falniowski A. 1987. Hydrobioidea of Poland (Prosobranchia: Gastropoda). Folia Malacol. 1: 1–122.
Falniowski A., Beran L. 2015. Belgrandiella A. J. Wagner, 1928 (Caenogastropoda: Truncatelloidea: Hydrobiidae): how many endemics? Folia Malacol. 23: 187–191.
Falniowski A., Pešić V., Glöer P. 2014. Montenegrospeum Pešić et Glöer, 2013: a representative of Moitessieriidae? Folia Malacol. 22: 263–268.
Falniowski A., Szarowska M. 2011. Radiation and­ phylogeography in a spring snail Bythinella (Mollusca: Gastropoda: Rissooidea) in continental Greece. Ann. Zool. Fenn. 48: 67–90.
Falniowski A., Szarowska M. 2012. Species distinctness of Lithoglyphus prasinus (Küster, 1852) (Rissooidea: Caenogastropoda). Folia Malacol. 20: 99–104.
Falniowski A., Szarowska M. 2013. Phylogenetic relationships of Dalmatinella fluviatilis Radoman, 1973 (Caenogastropoda: Rissooidea). Folia Malacol. 21: 1–7.
Falniowski A., Szarowska M., Glöer P., Pešić V. 2012a. Molecules vs. morphology in the taxonomy of the Radomaniola/Grossuana group of Balkan Rissooidea (Mollusca: Caenogastropoda). J. Conchol. 41: 19–36.
Falniowski A., Szarowska M., Glöer P., Pešić V., Georgiev D., Horsak M., Sirbu I. 2012b. Radiation in Bythinella (Mollusca: Gastropoda: Rissooidea) in the Balkans. Folia Malacol. 20: 1–9.
Falniowski A., Szarowska M., Sirbu I., Hillebrand A., Baciu M. 2008 Heleobia dobrogica (Grossu & Negrea, 1989) (Gastropoda: Rissooidea: Cochliopidae) and the estimated time of its isolation in a continental analogue of hydrothermal vents. Moll. Res. 28: 165–170.
Falniowski A., Wilke T. 2001. The genus Marstoniopsis (Gastropoda: Rissooidea): intra- and intergeneric phylogenetic relationships. J. Mollus. Stud. 67: 483–488.
Georgiev D., Osikowski A., Hofman S., Rysiewska A., Falniowski A. 2017. Contribution to the morphology of the Bulgarian stygobiont Truncatelloidea (Caenogastropoda). Folia Malacol. 25: 15–25.
Giusti F., Bodon M. 1984. Notulae Malacologicae, XXXI: Nuove Hydrobiidae dell’Italia nord-occidentale (Gastropoda: Prosobranchia). Arch. Molluskenkd. 114: 157–181.
Giusti F., Pezzoli E. 1980. Gasteropodi, 2 (Gastropoda: Prosobranchia; Hydrobioidea, Pyrguloidea). AQ/1/47, Guide per il riconoscimento delle specie animali delle acque interne Italiane 8. Consiglio Nazionale delle Ricerche, Verona.
Glöer P. 2002. Die Süsswassergastropoden Nord- und Mitteleuropas, Bestimmungsschlüssel, Lebensweise, Verbreitung. Die Tierwelt Deutschlands, vol. 73. Conchbooks, Hackenheim.
Haase M. 1993. Belgrandiella ganslmayri, a new hydrobiid species from Upper Austria (Caenogastropoda). Ann. Naturhist. Mus. Wien. 94/95B:181–186.
Haase M. 1994. Differentiation of selected species of Belgrandiella and the redefined genus Graziana (Gastropoda: Hydrobiidae). Zool. J. Linn. Soc. Lond. 111: 219–246.
Haase M. 1996. The radiation of spring snails of the genus Belgrandiella in Austria (Mollusca: Caenogastropoda: Hydrobiidae). Hydrobiologia 319: 119–129.
Haase M., Weigand E., Haseke H. 2000. Two new species of the family Hydrobiidae (Mollusca: Caenogastropoda) from Austria. Veliger 43: 179–189.
Hall T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acid. Symp. Ser. 41: 95–98.
Kabat A. R., Hershler R. 1993. The prosobranch snail family hydrobiidae (Gastropoda: Rissooidea): review of classification and supraspecific taxa. Smithsonian Contr. Zool. 547: 1–94.
Kantor Y. I., Vinarski M. V., Schileyko A. A., Sysoyev A. V. 2010. Continental molluscs of Russia and adjacent territories [Internet]. Version 2.3.1. [cited Dec 2013 12]. Available from:
Layton K. K., Martel A. L., Hebert P. D. 2014. Patterns of DNA barcode variation in Canadian marine molluscs. PLoS ONE 9 (4): E95003 (2014).
Miller M. A., Pfeiffer W., Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov, New Orleans, LA: 1–8.
Neretina T. V. 2014. Littorina littorea isolate C histone H3 (H3) gene, partial cds – KP113574 unpublished. Available from (accessed 18 November 2017)
Radoman P. 1973. New classification of fresh and brackish water Prosobranchia from the Balkans and Asia Minor. Posebna Izdanja, Prirodn. Mus. Beograd. 32: 1–30.
Radoman P. 1975. Specijacija u ookviru roda Belgrandiella i njemu srodnih rodova na Balkanskom poluostrvu. Glasnik Prirogdnjackog Museja, Beograd, series B. 30: 29–69.
Radoman P. 1983. Hydrobioidea a superfamily of Prosobranchia (Gastropoda). I. Systematics. Serbian Academy of Sciences and Arts, Monograph 547, Department of Sciences 57: 1–256.
Radoman P. 1985. Hydrobioidea, a superfamily of Prosobranchia (Gastropoda). II. Origin, zoogeography, evolution in the Balkans and Asia Minor. Faculty of Science – Department of Biology Monographs, 1, Institute of Zoology Beograd 1: 1–173.
Ronquist F., Teslenko M., van der Mark P., Ayres D. L., Darling A., Höhna S., Larget B., Liu L., Suchard M. A., Huelsenbeck J. P. 2012. Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542.
Rysiewska A., Georgiev D., Osikowski A., Hofman S., Falniowski A. 2016. Pontobelgrandiella Radoman, 1973 (Caenogastropoda: Hydrobiidae): A recent invader of subterranean waters? J. Conch. 42: 1–11.
Rysiewska A., Prevorčnik S., Osikowski A., Hofman S., Beran L. Falniowski A. 2017. Phylogenetic relationships in Kerkia and introgression between Hauffenia and Kerkia (Caenogastropoda: Hydrobiidae). J. Zool. Syst. Evol. Res. 55: 106–117.
Schütt H. 1980. Zur Kenntnis griechischer Hydrobiiden. Arch Molluskenkd. 110: 115–149.
Shadin V. I. 1932. Die Süßwassermollusken aus der Rion-Höhle bei Kutais (Transkaukasien, Georgien). Arch. Molluskenkd. 64: 12–14.
Shadin V. I. 1952. Mollusks of fresh and brackish waters of the USSR. Academy of Sciences of the U.S.S.R., Moscow, Leningrad.
Sitnikova T. Ya., Sysoev A. V., Kijashko P. V. 2017. Species of freshwater gastropods described by Ya. L. Starobogatov: Pulmonata (Acroloxidae), Heterobranchia (Valvatidae) and Caenogastropoda (Viviparoidea, Truncatelloidea and Cerithioidea). Proc. Zool. Inst. RAS 321: 247–299.
Stamatakis, A. 2014. RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.
Starobogatov Y. I. 1962. Contribution to molluscs from subterranean waters of the Caucasus. Byulleten Moskovskogo Obschchestva Ispytatelei Prirody, Otdel biologicheskiy 67: 42–54.
Szarowska M. 2006. Molecular phylogeny, systematics and morphological character evolution in the Balkan Rissooidea (Caenogastropoda). Folia Malacol. 14: 99–168.
Szarowska M., Falniowski A. 2008. There is no philosopher’s stone: coup de grace for the morphology-based systematics in the rissooidean gastropods? 5th Congress of the European Malacological Societies, Ponta Delgada: 28.
Szarowska M., Falniowski A. 2011. An unusual, flagellum-bearing hydrobiid snail (Gastropoda, Rissooidea, Hydrobiidae) from Greece, with descriptions of a new genus and a new species. J. Nat. Hist. 45: 2231–2246.
Szarowska M., Falniowski A. 2013a. Phylogenetic relationships of the Emmericiidae (Caenogastropoda: Rissooidea). Folia Malacol. 21: 67–72.
Szarowska M., Falniowski A. 2013b. Species distinctness of Sadleriana robici (Clessin, 1890) (Gastropoda: Rissooidea). Folia Malacol. 21: 127–133.
Szarowska M., Falniowski A. 2014a. Horatia Bour­guignat, 1887: is this genus really phylogenetically very close to Radomaniola Szarowska, 2006 (Caenogastropoda: Rissooidea). Folia Malacol. 22: 31–39.
Szarowska M., Falniowski A. 2014b. Ventrosia ­maritima (Milaschewitsch, 1916) and V. ventrosa (Montagu, 1803) in Greece: molecular data as a source of information about species ranges within the Hydrobiinae (Caenogastropoda: Truncatelloidea). Folia Malacol. 22: 61–67.
Szarowska M., Falniowski A., Šteffek J. 2011. Phylogenetic relationships of Alzoniella slovenica (Ložek & Brtek, 1964) (Caenogastropoda: Hydrobiidae). Folia Malacol. 19: 87–95.
Szarowska M., Grzmil P., Falniowski A., Sirbu I. 2007. Grossuana codreanui (Grossu, 1946) and the phylogenetic relationships of the East Balkan genus Grossuana (Radoman, 1973) (Gastropoda: Rissooidea). Hydrobiologia 579: 379–391.
Szarowska M., Hofman S., Osikowski A., Falniowski A. 2014a. Daphniola Radoman, 1973 (Caenogastropoda: Truncatelloidea) at east Aegean islands. Folia Malacol. 22: 269–275.
Szarowska M., Osikowski A., Hofman S., Falniowski A. 2016. Pseudamnicola Paulucci, 1878 (Caenogastropoda: Truncatelloidea) from the Aegean Islands: a long or short story? Org. Divers. Evol. 16: 121–139.
Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725–2729.
Tzvetkov B. N. 1940. A note on cave molluscs of Transcaucasia. Byulleten Moskovskogo Obshchestva Ispytatelei Prirody, otdel biologiya 49: 57–59.
Vinarski M. B., Kantor Yu. I. 2016. Analytical catalogue of fresh and brackish water molluscs of Russia and adjacent countries. Tovarishchestvo Nauchnyckh Izdanii KMK, Moscow.
Vinarski M. V., Palatov D. M., Glöer P. 2014. Revision of ‘Horatia’ snails (Mollusca: Gastropoda: Hydrobiidae sensu lato) from South Caucasus with description of two new genera. J. Nat. Hist. 48: 2237–2253.
Wagner A. 1927. Studien zur Molluskenfauna der Balkanhalbinsel mit besonderer Berücksichtigung Bulgariens und Thraziens, nebst monographischer Bearbeitung einzelner Gruppen. Ann. Zool. Mus. Pol. Hist. Nat. 6: 263–399.
Wilke T. 2003. Salenthydrobia gen. nov. (Rissooidea: Hydrobiidae): a potential relict of the Messinian salinity crisis. Zool. J. Linn. Soc. 137: 319–336.
Wilke T., Davis G. M. 2000. Infraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissoacea: Gastropoda): Do their different life histories affect biogeographic patterns and gene flow? Biol. J. Linn. Soc. 70: 89–105.
Wilke T., Davis G. M., Chen C. E., Zhou X.-N., Zeng X., P., Zhang Y., Spolsky C. M. 2000. Oncomelania hupensis (Gastropoda: Rissooidea) in eastern China: molecular phylogeny, population structure, and ecology. Acta Trop. 77: 215–227.
Wilke T., Davis G. M., Falniowski A., Giusti F., Bodon M. Szarowska M. 2001. Molecular systematics of Hydrobiidae (Mollusca: Gastropoda: Rissooidea): testing monophyly and phylogenetic relationships. Proc. Acad. Nat. Sci. Phil. 151: 1–21.[0001:MSOHMG]2.0.CO;2
Wilke T., Haase M., Hershler R., Liu H. P., Misof B., Ponder W. 2013. Pushing short DNA fragments to the limit: Phylogenetic relationships of ‘hydrobioid’ gastropods (Caenogastropoda: Rissooidea). Mol. Phylogenet. Evol. 66: 715–736.
Wilke T., Rolán E., Davis G. M. 2000. The mudsnail genus Hydrobia s. s. in the northern Atlantic and western Mediterranean: a phylogenetic hypothesis. Mar. Biol. 137: 827–833.
Xia X. 2000. Data analysis in molecular biology and evolution. Kluwer Academic Publishers, Boston, Dordrecht & London.
Xia X. 2013. DAMBE: A comprehensive software package for data analysis in molecular biology and evolution. Mol. Biol. Evol. 30: 1720–1728.
Xia X., Xie Z., Salemi M., Chen L., Wang Y. 2003. An index of substitution saturation and its application. Mol. Phylogenet. Evol. 26: 1–7.

Folia Malacologica (2017) 25: 237-247
First published on-line: 2017-12-01 00:00:00
Full text (.PDF) BibTeX Mendeley Back to list