Abstract
Species invasions into ancient lakes are an important but little understood phenomenon. At ancient Lake Ohrid, a systematic assessment of invasive mollusc species using morphological and genetic data was conducted from 2003 to 2012. Two globally invasive gastropod species, Physa acuta and Ferrissia fragilis, have recently been discovered at 4 out of 386 sites. These sites are anthropogenically impacted. The invasive species co-occur with endemics. Phylogenetic analyses of populations from native and invaded ranges of both species confirmed their identities and provided insights into their invasion histories. Accordingly, P. acuta is genetically more diverse than F. fragilis. Both species are currently present in a considerable number of lakes on the Balkan Peninsula. Possible future trends in Lake Ohrid and the Balkans are discussed and further spread of both species is likely. Given the ongoing environmental change in Lake Ohrid, the number of observations of non-indigenous or other widespread species will probably rise in the coming years and such species and their impact on native species should be carefully monitored. Moreover, ancient lakes with recurrent invasions of alien species might serve as interesting model systems for the study of important topics of invasion biology.
Similar content being viewed by others
References
Albrecht, C. & T. Wilke, 2008. Lake Ohrid: biodiversity and evolution. Hydrobiologia 615: 103–140.
Albrecht, C., T. Wilke, K. Kuhn & B. Streit, 2004. Convergent evolution of shell shape in freshwater limpets: the African genus Burnupia. Zoological Journal of the Linnean Society 140: 577–586.
Albrecht, C., C. Kroll & T. Wilke, 2009a. Invasion of ancient Lake Titicaca by the globally invasive Physa acuta (Gastropoda: Pulmonata: Hygrophila). Biological Invasions 11: 1821–1826.
Albrecht, C., K. Schreiber, T. Hauffe & T. Wilke, 2009b. Tracking biological invasions into ancient lakes: Physa acuta (Gastropoda: Hygrophila) on the Balkans. Review (Sbornik na rabotite) 42: 8–9.
Albrecht, C., T. Hauffe, K. Schreiber, S. Trajanovski & T. Wilke, 2009c. Mollusc biodiversity and endemism in the potential ancient Lake Trichonis, Greece. Malacologia 51: 357–375.
Albrecht, C., T. Hauffe, K. Schreiber & T. Wilke, 2012. Mollusc biodiversity in a European ancient lake system: lakes Prespa and Mikri Prespa in the Balkans. Hydrobiologia 682: 47–59.
Anderson, R., 2003. Physella (Costatella) acuta Draparnaud in Britain and Ireland – its taxonomy, origins and relationships to other introduced Physidae. Journal of Conchology 38: 7–21.
Bank, R. A., 2012. Fauna Europaea: Mollusca: Gastropoda. Fauna Europaea version 2.5. http://www.faunaeur.org.
Bousset, L., P.-Y. Henry, P. Sourrouille & P. Jarne, 2004. Population biology of the invasive freshwater snail Physa acuta approached through genetic markers, ecological characterization and demography. Molecular Ecology 13: 2023–2036.
DAISIE, 2009. Handbook of Alien Species in Europe. Springer, Dordrecht.
Dhora, D., 2002. The freshwater molluscs of Albania. In Dhora, D. (ed), Studies on the Molluscs of Albania. Camaj-Pipa, Shkodra: 115–130.
Dillon, R. T., A. R. Wethington, J. M. Rhett & T. P. Smith, 2002. Populations of the European freshwater pulmonate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra. Invertebrate Biology 121: 226–234.
Falkner, G. & T. von Proschwitz, 1998. A record of Ferrissia (Pettancylus) clessiniana (Jickeli) in Sweden, with remarks on the identity and distribution of the European Ferrissia species. Journal of Conchology 36: 39–40.
Fehér, Z. & Z. P. Erőss, 2009. Checklist of the Albanian mollusc fauna. Schriften zur Malakozoologie 25: 22–38.
Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
Frank, C., 1983. Beitrag zur Molluskenfauna der östlichen Mittelmeerländer. Teil I: Bericht über eine Gastropodenausbeute aus Griechenland (Makedonien, Thrakien) vom Sommer 1981. Abhandlungen Staatliches Museum für Tierkunde Dresden 9: 69–80.
Frogley, M. R. & R. C. Preece, 2004. A faunistic review of the modern and fossil molluscan fauna from lake Pamvotis, Ioannina, an ancient lake in NW Greece: implications for endemism in the Balkans. In Griffith, H. I., B. Kryštufek & J. M. Reed (eds), Balkan Biodiversity. Kluwer Academic Publishers, Dordrecht: 243–260.
Frogley, M. R. & R. C. Preece, 2007. A review of the aquatic Mollusca from Lake Pamvotis, Ioannina, an ancient lake in NW Greece. Journal of Conchology 39: 271–295.
Genner, M. J., E. Michel, D. Erpenbeck, N. de Voogd, F. Witte & J. P. Pointier, 2004. Camouflaged invasion of Lake Malawi by an Oriental gastropod. Molecular Ecology 13: 2135–2141.
Glöer, P. & V. Pešić, 2008. The freshwater gastropods of the Skadar Lake with the description of Valvata montenegrina n. sp. (Mollusca, Gastropoda, Valvatidae). In: Pacićević, D. & M. Perreau (eds), Advances in the Studies of the Subterranean and Epigean Fauna of the Balkan Peninsula. Volume dedicated to the memory of Guido Nonvellier. Monography, Institute for Nature Conservation of Serbia: 341–348.
Glöer, P. & V. Pešić, 2013. A new freshwater snail genus (Hydrobiidae, Gastropoda) from Montenegro, with a discussion on gastropod diversity and endemism in Skadar Lake. ZooKeys 281: 69–90.
Glöer, P. & I. Sîrbu, 2006. New freshwater molluscs species found in the Romanian fauna. Heldia 6: 229–238.
Glöer, P., C. Albrecht & T. Wilke, 2007. Enigmatic distribution patterns of the Bithyniidae in the Balkan region (Gastropoda: Rissooidea). Mollusca 25: 13–22.
Goudswaard, K. P., F. Witte & E. F. Katunzi, 2008. The invasion of an introduced predator, Nile perch (Lates niloticus, L.) in Lake Victoria (East Africa): chronology and causes. Environmental Biology of Fishes 81: 127–139.
Hall, T. A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
Hauffe, T., C. Albrecht, K. Schreiber, K. Birkhofer, S. Trajanovski & T. Wilke, 2011. Spatially explicit analysis of gastropod biodiversity in ancient Lake Ohrid. Biogeosciences 8: 175–188.
Heiler, K. C. M., N. Nahavandi & C. Albrecht, 2010. A new invasion into an ancient lake – the invasion history of the dreissenid mussel Mytilopsis leucophaeata (Conrad, 1831) and its first record in the Caspian Sea. Malacologia 53: 185–192.
Herder, F., U. K. Schliewen, M. F. Geiger, R. K. Hadiaty, S. M. Gray, J. S. McKinnon, R. P. Walter & J. Pfaender, 2012. Alien invasion in Wallace’s dreamponds: records of the hybridogenic “flowerhorn” cichlid in Lake Matano, with an annotated checklist of fish species introduced to the Malili Lakes system in Sulawesi. Aquatic Invasion 7: 521–535.
Huelsenbeck, J. P. & F. Ronquist, 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.
Jaeckel, S. G., W. Klemm & W. Meise, 1957. Die Land- und Süßwasser-Mollusken der nördlichen Balkanhalbinsel. Abhandlungen und Berichte des Museums Tierkunde und Völkerkunde zu Dresden 23: 141–205.
Jovanović, B. J., 1997. The Mollusca fauna of the Skadar Lake. Natural values and protection of Skadar Lake. Papers from a Symposium, Podgorica, November 8–9th, 1995: 263–277.
Kadolski, D., 2012. Nomenclatural comments on non-marine molluscs occurring in the British Isles. Journal of Conchology 41: 65–90.
Kappes, H. & P. Haase, 2012. Slow but steady: dispersal of freshwater molluscs. Aquatic Science 74: 1–14.
Käufle, F., 1930. Die schalentragenden Land- und Süßwassermollusken, Teil X. In Beier, M. (ed.), Zoologische Forschungsreise nach den Ionischen Inseln und dem Peloponnes. Sitzungsbericht der Mathematisch-Naturwissenschaftlichen Classe der Kaiserlichen Akademie der Wissenschaften Abteilung 1 139:161–188.
Kostoski, G., C. Albrecht, S. Trajanovski & T. Wilke, 2010. A freshwater biodiversity hotspot under pressure – assessing threats and identifying conservation needs for ancient Lake Ohrid. Biogeosciences 7: 3999–4015.
Marrone, F., S. Lo Brutto & M. Arculeo, 2011. Cryptic invasion in Southern Europe: the case of Ferrissia fragilis (Pulmonata: Ancylidae) Mediterranean populations. Biologia 66: 484–490.
Matzinger, A., Z. Spirkovski, S. Patceva & A. Wüest, 2006. Sensitivity of ancient Lake Ohrid to local anthropogenic impacts and global warming. Journal of Great Lakes Research 32: 158–179.
Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.
Radea, C., I. Louvrou & A. Economou-Amilli, 2008. First record of the New Zealand mud snail Potamopyrgus antipodarum J. E. Gray, 1843 (Mollusca: Hydrobiidae) in Greece – notes on its population structure and associated microalgae. Aquatic Invasions 3: 341–344.
Radoman, P., 1985. Hydrobioidea, a superfamily of Prosobranchia (Gastropoda), II Origin, Zoogeography, Evolution in the Balkans and Asia Minor. Monographs Institute of Zoology 1, Beograd.
Raposeiro, P. M., A. C. Costa & A. F. Martins, 2011. On the presence, distribution and habitat of the alien freshwater snail Ferrissia fragilis (Tyron, 1863) (Gastropoda: Planorbidae) in the oceanic islands of the Azores. Aquatic Invasion 6: 13–17.
Reischütz, A. & P. L. Reischütz, 2002. Hellenika pantoia, 1: Pyrgulidae (Gastropoda: Prosobranchia) aus dem Limni Pamvotis (Epirus, Griechenland). Nachrichtenblatt der Ersten Vorarlberger Malakologischen Gesellschaft 10: 1–4.
Reischütz, A. & P. L. Reischütz, 2003. Hellenika pantoia, 5: Zur Kenntnis der Molluskenfauna des Limni Trichonida und des Limni Lisimachia (Aitolien/Akarnien, Griechenland). Nachrichtenblatt der Ersten Vorarlberger Malakologischen Gesellschaft 11: 28–30.
Reischütz, A. & P. L. Reischütz, 2008. Hellenika pantoia, 18: Ein Beitrag zur Kenntnis der Molluskenfauna der böotischen Seen – Limni Yliki und Paralimni und ihre Umgebung (Zentral-Griechenland). Nachrichtenblatt der Ersten Vorarlberger Malakologischen Gesellschaft 15: 21–23.
Reischütz, P. L. & H. Sattmann, 1990. Beiträge zur Molluskenfauna des Epirus, 2. Annalen des Naturhistorischen Museums in Wien Serie B Botanik und Zoologie 91: 253–272.
Schütt, H., 1985. Die Mollusken des Vegoritis-Sees in Makedonien. Mitteilungen der Zoologischen Gesellschaft Braunau 12(13): 301–302.
Schütt, H., 1987. Limnische Mollusken aus älterem Quartär Makedoniens. Zoologische Mededelingen 61: 113–131.
Son, M. O., 2007. Native range of the zebra mussel and quagga mussel and new data on their invasion within the Ponto-Caspian region. Aquatic Invasions 2: 174–184.
Stanković, S., 1985. A contribution to the knowledge of gastropod fauna of Dojran Lake and the surrounding waters. Fragmenta Balcanica 13: 141–151.
Van Leeuwen, C. H. A., N. Huig, G. van der Velde, T. A. van Alen, C. A. M. Wagemarker, C. D. H. Sherman, M. Klaassen & J. Figuerola, 2013. How did this snail get here? Several dispersal vectors inferred for an aquatic invasive species. Freshwater Biology 58: 88–99.
Vardala-Theodorou, E., P. Polychronopoulos, P. Magiatis & A.-L. Skaltsounis, 2006. Contribution to the systematic and chemical study of malacofauna, of the Yliki-Paralimni lakes, Central Greece. Abstract, 10th Internationale Congress Zoogeographic & Ecology Greece Adjacent Regions, Patras, p. 122.
Walther, A. C., T. Lee, J. B. Burch & D. Ó. Foighil, 2006. Confirmation that the North American ancylid Ferrissia fragilis (Tryon, 1863) is a cryptic invader of European and East Asian freshwater ecosystems. Journal of Molluscan Studies 72: 318–321.
Walther, A. C., J. B. Burch & D. Ó. Foighil, 2010. Molecular phylogenetic revision of the freshwater limpet genus Ferrissia (Planorbidae: Ancylinae) in North America yields two species: Ferrissia (Ferrissia) rivularis and Ferrissia (Kincaidilla) fragilis. Malacologia 53: 25–45.
Wethington, A. R. & C. Lydeard, 2007. A molecular phylogeny of Physidae (Gastropoda: Basommatophora) based on mitochondrial DNA sequences. Journal of Molluscan Studies 73: 241–257.
Wilke, T., R. Schultheiß, C. Albrecht, N. Bornmann, S. Trajanovski & T. Kevrekidis, 2010. Native Dreissena freshwater mussels in the Balkans: in and out of ancient lakes. Biogeosciences 7: 3051–3061.
Wittmann, M. E., S. Chandra, J. E. Reuter, S. G. Schladow, B. C. Allen & K. J. Webb, 2012. The control of an invasive bivalve, Corbicula fluminea, using gas impermeable benthic barriers in a large natural lake. Environmental Management 49: 1163–1173.
Xia, X. & P. Lemey, 2009. Assessing substitution saturation with DAMBE. In Lemey, P., M. Salemi & A.-M. van Damme (eds), The Phylogenetic Handbook: A Practical Approach to DNA and Protein Phylogeny. Cambridge University Press, Cambridge: 615–630.
Xia, X., Z. Xie, M. Salemi, L. Chen & Y. Wang, 2003. An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26: 1–7.
Zukowski, S. & K. F. Walker, 2009. Freshwater snails in competition: alien Physa acuta (Physidae) and native Glyptophysa gibbosa (Planorbidae) in the River Murray, South Australia. Marine and Freshwater Research 60: 999–1005.
Acknowledgments
We are grateful to the colleagues who have supported our work in the Balkan countries, namely G. Kostoski, S. Trajanovski, D. Georgiev, A. Mogias, T. Kevrekidis, Z. Fehér, P. Glöer, V. Pešić. Special thanks go to the numerous students of the Wilke lab (Giessen) who took part in the field campaigns. We also particularly thank P. Reischütz for continuously sharing his knowledge on the Balkan malacofauna and for contributing valuable data to this paper. Z. Fehér is also gratefully acknowledged for providing important distributional records. C. Renker kindly donated Ferrissia specimens from Lake Kalodiki. We thank K. Heiler for helpful comments on an earlier version of this paper. The German Science Foundation (DFG AL 1076/3-1, WI 1902/8-2) supported our work on Lake Ohrid.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: T. von Rintelen, R. M. Marwoto, G. D. Haffner & F. Herder / Speciation in Ancient Lakes – Classic Concepts and New Approaches
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Albrecht, C., Föller, K., Clewing, C. et al. Invaders versus endemics: alien gastropod species in ancient Lake Ohrid. Hydrobiologia 739, 163–174 (2014). https://doi.org/10.1007/s10750-013-1724-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-013-1724-1