Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2016-03-30
Page range: 294–300
Abstract views: 88
PDF downloaded: 1

A note on the biogeographical origin of the brine shrimp Artemia urmiana Günther, 1899 from Urmia Lake, Iran

Honey bee Research and Extension Laboratory (HBREL), Department of Entomology and Nematology, 970 Natural Area Drive, University of Florida, Gainesville, Florida, 32611, United States of America
Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China
Institut Méditerranéen d'Ecologie et de Paléoécologie UMR 6116 du CNRS-Europôle Méditerranéen de l'Arbois-Pavillon Villemin–BP 80, 13545 Aix-en-Provence Cedex 04, France
Institute of Pharmacy and Molecular Biotechnology (IPMB), Heidelberg University, Im Neuenheimer Feld 364 D–69120, Heidelberg, Germany
Crustacea Biogeographical origin Artemia urmiana Iran Ukraine

Abstract

The brine shrimp Artemia urmiana, an abundant inhabitant of the hypersaline Urmia Lake in northwestern Iran, has recently been described from Lake Koyashskoe, also a shallow hypersaline lake that is located on the Black Sea coast of the Crimean Peninsula (Ukraine). This discovery has questioned the endemicity of A. urmiana in Urmia Lake and has also brought into question the biogeographical origin of this species. In the present study, we combined recent genetic divergence data (mtDNA-COI) with palaeoecological evidence to address the biogeographical origin of A. urmiana. Calibration of the molecular clock of the COI region was set by assigning the age of the micro-crustacean Daphnia pulex minimally at 145 Mya. The divergence age of A. urmiana in Urmia Lake dates back to 383,000 years, whereas Ukrainian Artemia reflects a very young populations that diverged about 196,000 years ago. Palaeoecological evidence suggests that the age of the major habitat of A. urmiana i.e. Urmia Lake goes back to the Tertiary Period while the Ukranian habitats of the species are very young, by virtue of geological features of the Holocene age. We conclude that the biogeographical origin of A. urmiana is outside of Europe and the current state of knowledge strongly suggests that Urmia Lake has been the major source of its expansion into its modern habitats in Europe.

 

References

  1. Abatzopoulos, T.J., Amat, F., Baxevanis, A.D., Belmonte, G., Hontoria, F., Maniatsi, S. Moscatello, S., Mura, G. & Shadrin, N. (2009) Updating geographic distribution of Artemia urmiana Günther, 1890 (Branchiopoda: Anostraca) in Europe: an integrated and interdisciplinary approach. International Review of Hydrobiology, 94, 560–579.
    http://dx.doi.org/10.1002/iroh.200911147

    Anufriieva, E.V. & Shadrin, N.V. (2012) Artemia urmiana Gunther, 1900 (Anostraca): historical biogeography, its possible future in Lake Urmia, and perspectives for aquaculture. In: First International Conference on Larviculture in Iran and International Workshop on Replacement of Fish Meal/Oil with Plant Sources, 2012, pp. 784−789. [Karaj, Iran]

    Asem, A., Rastegar-Pouyani, N. & Agh, N. (2007) Biometrical study of Artemia urmiana (Anostraca: Artemiidae) cysts harvested from Lake Urmia (West Azerbaijan, Iran). Turkish Journal of Zoology, 31, 171−180.

    Asem, A. (2008) Historical record on brine shrimp Artemia more than one thousand years ago from Urmia Lake, Iran. Journal of Biological Research, 9, 113−114.

    Asem, A., Atashbar, B., Rastegar-Pouyani, N. & Agh, N. (2009) Biometric comparison of two parthenogenetic populations of Artemia Leach, 1819 from the Urmia Lake basin, Iran (Anostraca: Artemiidae). Zoology in the Middle East, 47, 117−120.
    http://dx.doi.org/10.1080/09397140.2009.10638358

    Asem, A., Rastegar-Pouyani, N. & De los Rios, P. (2010) The genus Artemia Leach, 1819 (Crustacea: Branchiopoda): true and false taxonomical descriptions. Latin American Journal of Aquatic Research, 38, 501−506.

    Asem, A. & Rogers, D.C. (2012) Clarification of the publication date for Artemia urmiana Günther (Crustacea: Anostraca): 1890, 1899 or 1900? International Journal of Artemia Biology, 2, 3−6.

    Clark, L.S. & Bowen, S.T. (1976) The genetics of Artemia salina. VII. Reproductive isolation. Journal of Heredity, 67, 385−388.

    Djamali, M. (2008) Changements paléoenvironnementaux en Iran au cours des deux derniers cycles climatiques (végétation-climat-anthropisation). Unpublished PhD thesis, Aix-Marseille Université. [unkown pagination, in both English and French]

    Djamali, M., de Beaulieu, J.L., Shah-Hosseini, M., Andrieu-Ponel, V., Amini, A., Akhani, H., Leroy, S.A.G., Stevens, L., Alizadeh, H., Ponel, P. & Brewer, S. (2008a) A late Pleistocene long pollen record from Lake Urmia, NW Iran. Quaternary Research, 69, 413−420.
    http://dx.doi.org/10.1016/j.yqres.2008.03.004

    Djamali, M., Kürschner, H., Akhani, H., de Beaulieu, J.L., Amini, A., Andrieu-Ponel, V., Ponel, P. & Stevens, L. (2008b) Palaeoecological significance of the spores of the liverwort Riella (Riellaceae) in a late Pleistocene long pollen record from the hypersaline Lake Urmia, NW Iran. Review of Palaeobotany and Palynology, 152, 66−73.
    http://dx.doi.org/10.1016/j.revpalbo.2008.04.004

    Djamali, M., Ponel, P., Delille, T., Thiéry, A., Asem, A., Andrieu-Ponel, V., de Beaulieu, J.L., Lahijani, H., Shah-Hosseini, M., Amini, A. & Stevens, L. (2010) A 200,000-year record of Artemia remains (Crustacea, Anostraca) in Lake Urmia, NW Iran. International Journal of Aquatic Sciences, 1, 14−18.

    Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
    http://dx.doi.org/10.1186/1471-2148-7-214

    Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29, 1969−1973.
    http://dx.doi.org/10.1093/molbev/mss075

    Eimanifar, A. & Mohebbi, F. (2007) Urmia Lake (Northwest Iran): A brief review. Saline Systems, 3, 1–8.
    http://dx.doi.org/10.1186/1746-1448-3-5

    Eimanifar, A. & Wink, W. (2013) Fine-scale population genetic structure in Artemia urmiana (Günther, 1890) based on mtDNA sequences and ISSR genomic fingerprinting. Organisms Diversity and Evolution, 13, 531–543.
    http://dx.doi.org/10.1007/s13127-013-0135-5

    Eimanifar, A., Van Stappen, G. & Wink, M. (2015) Geographical distribution and evolutionary divergence times of Asian populations of the brine shrimp Artemia (Crustacea, Anostraca). Zoological Journal of Linnean Society, 174, 447–458.
    http://dx.doi.org/10.1111/zoj.12242

    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.

    Khomenko, S.V. & Shadrin, N.V. (2009) Iranian endemic Artemia urmiana in hypersaline Lake Koyashskoe (Crimea, Ukraine): a preliminary discussion of introduction by birds. Branta. Transaction of Azov-Black Sea ornithological station, 12, 81–91.

    Kotov, A.A. & Taylor, D.J. (2011) Mesozoic fossils (>145 Mya) suggest the antiquity of the subgenera of Daphnia and their coevolution with chaoborid predators. BMC Evolutionary Biology, 11, 129.
    http://dx.doi.org/10.1186/1471-2148-11-129

    Lericolais, G., Popescu, I., Guichard, F. & Popescu, S.M. (2007) A Black Sea lowstand at 8500 yr B.P. Indicated by a relict coastal dune system at a depth of 90 m below sea level. GSA Special Papers, 426, 171−188.
    http://dx.doi.org/10.1130/2007.2426(12)

    Lericolais, G., bulois, C., Gillet, H. & Guichard, F. (2009) High frequency sea level fluctuations recorded in the Black Sea since the LGM. Global and Planetary Change, 66, 65−75.
    http://dx.doi.org/10.1016/j.gloplacha.2008.03.010

    Maknood, A.A.A. (2011) Ecological and biological study of the genus Artemia (L.) (Class Crustacea: Order Anostraca) in Iraq. Ph.D. Thesis. Mustansoria University. Baghdad. [unknown pagination]

    Manaffar, R., Zare, S., Agh, N., Siyabgodsi, A., Soltanian, S., Mees, F. & Van Stappen, G. (2011) Sediment cores from Lake Urmia (Iran) suggest the inhabitation by parthenogenetic Artemia around 5,000 years ago. Hydrobiologia, 671, 65−74.
    http://dx.doi.org/10.1007/s10750-011-0704-6

    Martin, R.E., Leorri, E. & McLaughlin, P.P. (2007) Holocene sea level and climate change in the Black Sea: multiple marine incursions related to freshwater discharge events. Quaternary International, 167, 61−72.
    http://dx.doi.org/10.1016/j.quaint.2006.11.003

    McMaster, K., Savage, A., Finston, T., Johnson, M.S. & Knott, B. (2007) The recent spread of Artemia parthenogenetica in Western Australia. Hydrobiologia, 576, 39−48.
    http://dx.doi.org/10.1007/s10750-006-0291-0

    Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256.
    http://dx.doi.org/10.1093/molbev/msn083

    Salman, S.D., Mohammed, D.S. & Ali, M.H. (2012) Review of the biogeography of Artemia Leach, 1819 (Crustacea: Anostraca) in Iraq. International Journal of Artemia Biology, 2, 62−73.

    Shadrin, N.V., Batogova, E.A., Belmonte, G., Moscatello, S., Litvinchuk, L.F. & Shadrina, S.V. (2008) Artemia urmiana Günther, 1890 (Anostraca, Artemiidae) in Koyashakoye Lake (Crimea, Black Sea) - a first finding out Urmia Lake (Iran). Marine Ecological Journal, 7, 30–31.

    Shadrin, N.V. & Batogova, E.A. (2009) Artemia urmiana Günther, 1890 (Anostraca, Artemiidae) in the Crimean lakes. Proceedings of the International Symposium, Urmia (Iran), 2009, 10−12.

    Shadrin, N. & Anufriieva, E. (2012) Review of the biogeography of Artemia Leach, 1819 (Crustacea: Anostraca) in Russia. International Journal of Artemia Biology, 2, 51−61.

    Shadrin, N., Anufriieva, E. & Galagovets, E. (2012) Distribution and historical biogeography of Artemia leach, 1819 (Crustacea: Anostraca) in Ukraine. International Journal of Artemia Biology, 2, 30−42.

    Stevens, L.R., Djamali, M., Andrieu-Ponel, V. & de Beaulieu, J.L. (2012) Hydroclimatic variations over the last two climatic cycles at Lake Urmia, Iran. Journal of Paleolimnology, 47, 645–660.
    http://dx.doi.org/10.1007/s10933-012-9588-3

    Subetto, D.A., Stolba, V., Neustrueva, I.Y., Sapelko, T.V., Kuznetsov, D.D., Gerasimenko, N., Bakhmutov, V., Ludikova, A.V. & Davydova, N.N. (2007) Environmental and Black Sea level changes in the Holocene as recorded in lakes Saki and Dzarylgach, Crimean Peninsula. Extended Abstract in IGCP 521 and 481. Gelendzhik (Russia) & Kerch (Ukraine). Rosselkhozakademiya Printing House, Moscow, pp. 157–159.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution, 30, 2725‒2729.
    http://dx.doi.org/10.1093/molbev/mst197

    Van Stappen, G. (2002) Zoogeography. In: Abatzopoulos, T.J., Beardmore, J.A., Clegg, J.S. & Sorgeloos, P. (Eds.), Artemia: Basic and Applied Biology. Kluwer Academic Publishers, Dordrecht, pp. 171–224.
    http://dx.doi.org/10.1007/978-94-017-0791-6_4

    Van Stappen, G., Yu, H., Wang, X., Hoffman, S., Cooreman, K., Bossier, P. & Sorgeloos, P. (2007) Occurrence of allochthonous Artemia species in the Bohai Bay area, PR China, as confirmed by RFLP analysis and laboratory culture tests. Fundamental and Applied Limnology, 170, 21–28.
    http://dx.doi.org/10.1127/1863-9135/2007/0170-0021

    Winguth, C., Wong, H.K., Panin, N., Dinu, C., Georgescu, P., Ungureanu, G., Krugliakov, V.V. & Podshuveit, V. (2000) Upper Quaternary water level history and sedimentation in the northwestern Black Sea. Marine Geology, 167, 127–146.
    http://dx.doi.org/10.1016/S0025-3227(00)00024-4