, Volume 715, Issue 1, pp 51–62 | Cite as

At the edge and on the top: molecular identification and ecology of Daphnia dentifera and D. longispina in high-altitude Asian lakes

  • Markus Möst
  • Adam Petrusek
  • Ruben Sommaruga
  • Petr Jan Juračka
  • Miroslav Slusarczyk
  • Marina Manca
  • Piet Spaak


The occurrence of members of the highly diverse Daphnia longispina complex in Southern and Central Asian high-mountain lakes has been recognized for more than a century. Until now, however, no molecular data have been available for these populations inhabiting the “Roof of the World.” Here, we present the first identification for D. gr. longispina from that region based on a molecular phylogeny. Our findings show that alpine lakes in the Pamir and Himalaya mountains host populations of widespread species of the complex, for which these are the highest known localities. A spineless morph from the Himalaya region, previously labeled as D. longispina var. aspina, was clustering tightly with D. dentifera, while a population from the Pamir mountain range was grouped with D. longispina. In addition, we analyzed ecological data available for lakes in the Khumbu region (Himalaya) to investigate ecological preferences of non-pigmented D. gr. longispina. The identified factors can at least partly be related to avoidance of high UV conditions by this species. We conclude that the widespread species D. dentifera and D. longispina also colonized the Asian high-mountain lakes, and identify the need for further research to trace the possible effect of rapid environmental changes in this region on the diversity and ecology of high-altitude Daphnia populations.


Daphnia longispina complex Alpine lakes Molecular systematics UV radiation 12S 



We thank Nicola Rhyner for technical assistance in the lab. We are grateful to Seiji Ishida for providing ND2 sequences, Christoph Tellenbach for statistical advice, Patrick Turko for proofreading, and two anonymous reviewers for their valuable comments. MM and PS were supported by the Swiss Science Foundation (CR3213_125211), AP and PJJ by the Czech Science Foundation (Project No. P506/10/P167) and the Grant Agency of the Charles University (1325/2010). The logistics for the field work at the Pyramid Research Laboratory was supported by a project granted to RS by the Committee on High Altitude Scientific and Technological Research (Ev-K²-CNR) in collaboration with the Nepal Academy of Science and Technology, and thanks to contributions from the Italian National Research Council and the Italian Ministry of Foreign Affairs. Phylogenetic analyses were performed with the help of the Genetic Diversity Centre of ETH Zurich.

Supplementary material

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Supplementary material 1 (PDF 65 kb)
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  1. Billiones, R., M. Brehm, J. Klee & K. Schwenk, 2004. Genetic identification of Hyalodaphnia species and interspecific hybrids. Hydrobiologia 526: 43–53.CrossRefGoogle Scholar
  2. Brede, N., A. Thielsch, C. Sandrock, P. Spaak, B. Keller, B. Streit & K. Schwenk, 2006. Microsatellite markers for European Daphnia. Molecular Ecology Notes 6: 536–539.CrossRefGoogle Scholar
  3. Brehm, V. & R. Woltereck, 1939. Die Daphniden der Yale–Northindia-Expedition. Internationale Revue der gesamten Hydrobiologie und Hydrographie 39: 1–19.CrossRefGoogle Scholar
  4. Cruz, R. V., H. Harasawa, M. Lal, S. Wu, Y. Anokhin, B. Punsalmaa, Y. Honda, M. Jafari, C. Li & N. Huu Ninh, 2007. Asia climate change 2007: impacts, adaptation and vulnerability. In Parry, M. L., O. F. Canziani, J. P. Palutikof, P. J. van der Linden, C. E. Hanson (eds), Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge: 469–506.Google Scholar
  5. Daday, E., 1908. Entomostraca et Hydrachnidae e Tibet. Records of the Indian Museum 2: 223–341.Google Scholar
  6. Dlouhá, Š., A. Thielsch, R. H. S. Kraus, J. Seda, K. Schwenk & A. Petrusek, 2010. Identifying hybridizing taxa within the Daphnia longispina species complex: a comparison of genetic methods and phenotypic approaches. Hydrobiologia 643: 107–122.CrossRefGoogle Scholar
  7. Dufresne, F., S. Marková, R. Vergilino, M. Ventura & P. Kotlík, 2011. Diversity in the reproductive modes of European Daphnia pulicaria deviates from the geographical parthenogenesis. PLoS One 6: e20049.PubMedCrossRefGoogle Scholar
  8. Dumont, H. J. & I. Velde, 1977. Report on a collection of Cladocera and Copepoda from Nepal. Hydrobiologia 53: 55–65.CrossRefGoogle Scholar
  9. Giardino, C., A. Oggioni, M. Bresciani & H. Yan, 2010. Remote sensing of suspended particulate matter in Himalayan lakes. Mountain Research and Development 30: 157–168.CrossRefGoogle Scholar
  10. Glagolev, S. M., 1995. Rod Daphnia. In Alexeev, V. R. (ed.), Key to Freshwater Invertebrates of Russia and Adjacent Lands, 2. Crustaceans. Zoological Institute, Russian Academy of Sciences, St. Petersburg: 48–58 [in Russian].Google Scholar
  11. Hamrová E., M. Krajicek, T. Karanovic, M. Černý & A. Petrusek, 2012. Congruent patterns of lineage diversity in two species complexes of planktonic crustaceans, Daphnia longispina (Cladocera) and Eucyclops serrulatus (Copepoda), in East European mountain lakes. Zoological Journal of the Linnean Society. doi: 10.1111/j.10963642.2012.00864.x.
  12. Hutchinson, E. G., 1937. Limnological studies in Indian Tibet. Internationale Revue der gesamten Hydrobiologie und Hydrographie 35: 134–177.CrossRefGoogle Scholar
  13. Ishida, S. & D. J. Taylor, 2007a. Mature habitats associated with genetic divergence despite strong dispersal ability in an arthropod. BMC Evolutionary Biology 7: 52.PubMedCrossRefGoogle Scholar
  14. Ishida, S. & D. J. Taylor, 2007b. Quaternary diversification in a sexual Holarctic zooplankter, Daphnia galeata. Molecular Ecology 16: 569–582.PubMedCrossRefGoogle Scholar
  15. Ishida, S., A. A. Kotov & D. J. Taylor, 2006. A new divergent lineage of Daphnia (Cladocera: Anomopoda) and its morphological and genetical differentiation from Daphnia curvirostris Eylmann, 1887. Zoological Journal of the Linnean Society 146: 385–405.CrossRefGoogle Scholar
  16. Ishida, S., A. Takahashi, N. Matsushima, J. Yokoyama, W. Makino, J. Urabe & M. Kawata, 2011. The long-term consequences of hybridization between the two Daphnia species, D. galeata and D. dentifera, in mature habitats. BMC Evolutionary Biology 11: 209.PubMedCrossRefGoogle Scholar
  17. Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120.PubMedCrossRefGoogle Scholar
  18. Kirk, K. L., 1991. Inorganic particles alter competition in grazing plankton – the role of selective feeding. Ecology 72: 915–923.CrossRefGoogle Scholar
  19. Koenings, J. P., R. D. Burkett & J. M. Edmundson, 1990. The exclusion of limnetic Cladocera from turbid glacier-meltwater lakes. Ecology 71: 57–67.CrossRefGoogle Scholar
  20. Kořínek, V., 1999. A guide to the identification of limnetic species of Cladocera in African inland waters. Occasional Publications SIL 1: 1–60.Google Scholar
  21. Kotov, A. A., A. Y. Sinev & V. L. Berrios, 2010. The Cladocera (Crustacea: Branchiopoda) of six high altitude water bodies in the North Chilean Andes, with discussion of Andean endemism. Zootaxa 2430: 1–66.Google Scholar
  22. Lacoul, P. & B. Freedman, 2005. Physical and chemical limnology of 34 lentic waterbodies along a tropical-to-alpine altitudinal gradient in Nepal. International Review of Hydrobiology 90: 254–276.CrossRefGoogle Scholar
  23. Löffler, H., 1969. High altitude lakes in Mt. Everest region. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 17: 373–385.Google Scholar
  24. Manca, M. & P. Comoli, 2004. Reconstructing long-term changes in Daphnia’s body size from subfossil remains in sediments of a small lake in the Himalayas. Journal of Paleolimnology 32: 95–107.CrossRefGoogle Scholar
  25. Manca, M., P. Cammarano & T. Spagnuolo, 1994. Notes on Cladocera and Copepoda from high-altitude lakes in the Mount Everest Region (Nepal). Hydrobiologia 287: 225–231.CrossRefGoogle Scholar
  26. Manca, M., D. Ruggiu, P. Panzani, A. Asioli, G. Mura & A. M. Nocentini, 1998. Report on a collection of aquatic organisms from high mountain lakes in the Khumbu Valley (Nepalese Himalayas). Memorie dell’Istituto Italiano di Idrobiologia 57: 77–98.Google Scholar
  27. Manuilova, E. F., 1964. Vetvistousye rachki (Cladocera) fauny SSSR. Opredeliteli po Faune SSSR, Vol. 88. Nauka, Moscow [in Russian].Google Scholar
  28. Mergeay, J., X. Aguilera, S. Declerck, A. Petrusek, T. Huyse & L. De Meester, 2008. The genetic legacy of polyploid Bolivian Daphnia: the tropical Andes as a source for the North and South American D. pulicaria complex. Molecular Ecology 17: 1789–1800.PubMedCrossRefGoogle Scholar
  29. Montero-Pau, J., A. Gomez & J. Munoz, 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.CrossRefGoogle Scholar
  30. Nilssen, J. P., A. Hobæk, A. Petrusek & M. Skage, 2007. Restoring Daphnia lacustris G.O. Sars, 1862 (Crustacea, Anomopoda): a cryptic species in the Daphnia longispina group. Hydrobiologia 594: 5–17.CrossRefGoogle Scholar
  31. Petrusek, A., M. Černý, J. Mergeay & K. Schwenk, 2007. Daphnia in the Tatra Mountain lakes: multiple colonisation and hidden species diversity revealed by molecular markers. Fundamental and Applied Limnology 169: 279–291.CrossRefGoogle Scholar
  32. Petrusek, A., A. Hobæk, J. P. Nilssen, M. Skage, M. Černý, N. Brede & K. Schwenk, 2008. A taxonomic reappraisal of the European Daphnia longispina complex (Crustacea, Cladocera, Anomopoda). Zoologica Scripta 37: 507–519.CrossRefGoogle Scholar
  33. Petrusek, A., A. Thielsch & K. Schwenk, 2012. Mitochondrial sequence variation suggests extensive cryptic diversity within the Western Palearctic Daphnia longispina complex. Limnology and Oceanography, in press.Google Scholar
  34. R Development Core Team, 2012. R: a language and environment for statistical computing, 2.14th ed. R Foundation for Statistical Computing, Vienna.Google Scholar
  35. Rellstab, C. & P. Spaak, 2007. Starving with a full gut? Effect of suspended particles on the fitness of Daphnia hyalina. Hydrobiologia 594: 131–139.CrossRefGoogle Scholar
  36. Rylov, M., 1930. Cladocera et Copepoda. In Abhandlungen der Pamir-Expedition 1928. II. Zoologie: 105–133.Google Scholar
  37. Sars, G. O., 1903. On the Crustacean fauna of Central Asia II. Annuaire du Musée Zoologique de l’Academie Imperiale des Sciences de St-Petersbourg 8: 157–194, 233–264, VIII pl.Google Scholar
  38. Schwenk, K., A. Sand, M. Boersma, M. Brehm, E. Mader, D. Offerhaus & P. Spaak, 1998. Genetic markers, genealogies and biogeographic patterns in the cladocera. Aquatic Ecology 32: 37–51.CrossRefGoogle Scholar
  39. Sharma, C., S. Sharma, R. Bajracharya, S. Gurung, I. Jüttner, S. Kang, Q. Zhang & Q. Li, 2012. First results on bathymetry and limnology of high-altitude lakes in the Gokyo Valley, Sagarmatha (Everest) National Park, Nepal. Limnology 13: 181–192.CrossRefGoogle Scholar
  40. Skage, M., A. Hobæk, Š. Ruthová, B. Keller, A. Petrusek, J. Seda & P. Spaak, 2007. Intra-specific rDNA-ITS restriction site variation and an improved protocol to distinguish species and hybrids in the Daphnia longispina complex. Hydrobiologia 594: 19–32.CrossRefGoogle Scholar
  41. Sommaruga, R., 2001. The role of solar UV radiation in the ecology of alpine lakes. Journal of Photochemistry and Photobiology B: Biology 62: 35–42.CrossRefGoogle Scholar
  42. Sommaruga, R., 2010. Preferential accumulation of carotenoids rather than of mycosporine-like amino acids in copepods from high altitude Himalayan lakes. Hydrobiologia 648: 143–156.CrossRefGoogle Scholar
  43. Sommaruga, R. & E. O. Casamayor, 2009. Bacterial ‘cosmopolitanism’ and importance of local environmental factors for community composition in remote high-altitude lakes. Freshwater Biology 54: 994–1005.CrossRefGoogle Scholar
  44. Spaak, P., J. Fox & N. G. Hairston, 2012. Modes and mechanisms of a Daphnia invasion. Proceedings of the Royal Society B 279: 2936–2944.PubMedCrossRefGoogle Scholar
  45. Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.PubMedGoogle Scholar
  46. Tamura, K., M. Nei & S. Kumar, 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences of the United States of America 101: 11030–11035.PubMedCrossRefGoogle Scholar
  47. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.PubMedCrossRefGoogle Scholar
  48. Tartari, G. A., P. Panzani, L. Adreani, A. Ferrero & C. De Vito, 1998. Lake cadastre of Khumbu Himal Region: geographical–geological–limnological data base. Memorie dell’ Istituto Italiano di Idrobiologia 57: 151–235.Google Scholar
  49. Taylor, D. J., P. D. N. Hebert & J. K. Colbourne, 1996. Phylogenetics and evolution of the Daphnia longispina group (Crustacea) based on 12S rDNA sequence and allozyme variation. Molecular Phylogenetics and Evolution 5: 495–510.PubMedCrossRefGoogle Scholar
  50. Taylor, D. J., H. L. Sprenger & S. Ishida, 2005. Geographic and phylogenetic evidence for dispersed nuclear introgression in a daphniid with sexual propagules. Molecular Ecology 14: 525–537.PubMedCrossRefGoogle Scholar
  51. Uéno, M., 1937. Cladocera of Manchoukuo. Internationale Revue der gesamten Hydrobiologie und Hydrographie 35: 199–216.CrossRefGoogle Scholar
  52. Van Damme, K. & H. Eggermont, 2011. The Afromontane Cladocera (Crustacea: Branchiopoda) of the Rwenzori (Uganda–D. R. Congo): taxonomy, ecology and biogeography. Hydrobiologia 676: 57–100.CrossRefGoogle Scholar
  53. Vereschagin, G. Yu., 1923. Zametka o presnovodnoi faune Pamira. Notiz über die Süsswasserfauna des Pamirs. Izvestii Rossijskogo gidrobiologicheskogo instituta 6: 21–40. [in Russian with German summary].Google Scholar
  54. Winder, M. & P. Spaak, 2001. Carbon as an indicator of Daphnia condition in an alpine lake. Hydrobiologia 442: 269–278.CrossRefGoogle Scholar
  55. Winder, M., H. R. Bürgi & P. Spaak, 2003. Mechanisms regulating zooplankton populations in a high-mountain lake. Freshwater Biology 48: 795–809.CrossRefGoogle Scholar
  56. Wolf, H. G. & M. A. Mort, 1986. Interspecific hybridization underlies phenotypic variability in Daphnia populations. Oecologia 68: 507–511.CrossRefGoogle Scholar
  57. Zuykova, E. I., A. S. Semenova, N. A. Bochkarev & A. V. Katokhin, 2010. Morphological differentiation, mitochondrial and nuclear DNA variability between geographically distant populations of Daphnia galeata and Daphnia cucullata (Anomopoda, Daphniidae). Journal of Siberian Federal University. Biology 3: 434–443.Google Scholar
  58. Zuykova, E. I., N. A. Bochkarev & A. V. Katokhin, 2012. Molecular genetic identification and phylogeny of Daphnia species (Crustacea: Cladocera) from the water bodies of Chany Lake basin. Russian Journal of Genetics, in press.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Markus Möst
    • 1
    • 2
  • Adam Petrusek
    • 3
  • Ruben Sommaruga
    • 4
  • Petr Jan Juračka
    • 3
  • Miroslav Slusarczyk
    • 5
  • Marina Manca
    • 6
  • Piet Spaak
    • 1
    • 2
  1. 1.Swiss Federal Institute of Aquatic Science and Technology, EawagDübendorfSwitzerland
  2. 2.Institute of Integrative BiologyETH ZürichZurichSwitzerland
  3. 3.Faculty of Science, Department of EcologyCharles University in PraguePrague 2Czech Republic
  4. 4.Laboratory of Aquatic Photobiology and Plankton Ecology, Institute of EcologyUniversity of InnsbruckInnsbruckAustria
  5. 5.Department of HydrobiologyUniversity of WarsawWarsawPoland
  6. 6.CNR Institute for Ecosystem Studies (ISE)Research Unit of Hydrobiology and Freshwater EcologyVerbania PallanzaItaly

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