pp 1–10 | Cite as

Does the dispersal of fairy shrimps (Branchiopoda, Anostraca) reflect the shifting geographical distribution of freshwaters since the late Mesozoic?

  • Hidetoshi NaganawaEmail author
  • Elena Yu. Naumova
  • Natalia N. Denikina
  • Ilya G. Kondratov
  • Elena V. Dzyuba
  • Atsushi Iwasawa
Special Feature: Original Article Freshwater Ecosystems - Key Problems and New Findings from Russian Lakes including Lake Baikal


Order Anostraca (fairy shrimp of large branchiopods) is a primitive crustacean group, retaining ancient forms and ecology. The Holarctic family Chirocephalidae originated over 100 million years ago; it is a very long-lived freshwater taxon that has survived from the Mesozoic to the present. Thus, using this taxon as an indicator, we verified how the geographical distribution of freshwaters shifted during the ancient era. We used newly collected samples of Drepanosurus uchidai from Aomori (northern Japan) and Galaziella baikalensis and Branchinecta orientalis from Olkhon Island (the largest lake-bound island of Lake Baikal, Russia) to sequence 658 bp of COI gene. These sequences, plus those of 16S rRNA gene (~ 550-bp mt16S rDNA fragment), were compared with those retrieved from GenBank. To re-evaluate and clarify phylogenetic relationships among the Chirocephalidae that remains confused till now, six genera of the family, including Polyartemiella, Drepanosurus, Eubranchipus, Chirocephalus, Artemiopsis, and Galaziella species were used for molecular analyses. Small water bodies usually have comparatively short lives and fade away sooner or later due to growth of aquatic plants and accumulation of bottom sediments. In such environments, refugia formed on the shores of large-scale lakes were necessary for large branchiopods to survive several Ice Ages. The lake shorelines have moved with the growth or decline of the lakes, but the habitats of large branchiopods sporadically left behind can now be confirmed as a history of the shifting geographical distribution of global freshwaters. For example, two types of large branchiopod populations from island-bound water bodies on Olkhon Island are recognized: (1) populations on the northwestern coast that are closely related to the group in the Mongolian Gobi steppe region, and (2) populations in other areas distant from the coast that are highly endemic to the island. Based on fossil records and genetic distances, an absolute differentiation time of world chirocephalids can be estimated as 140 million years ago in the Mesozoic era. On the other hand, the age of Lake Baikal is only 25‒30 million years at the most. Therefore, extant large branchiopods of Olkhon Island must have first appeared near the present lake catchment after separation from their ancestral populations that had originated in Europe, and before the formation of Lake Baikal.


Large branchiopods Fairy shrimp Drepanosurus Galaziella Olkhon Island (Lake Baikal) 



This paper is dedicated with pleasure to the memory of our late colleague, an excellent scientific interpreter, Ms. Galina Ivanovna Nagornaya. We are grateful to the organizers of the International Conference FEKP-2018 (Irkutsk, Russia) for inviting us and acknowledge the grant from The United Graduate School of Agricultural Science, Gifu University, Japan which allowed H.N.’s participation in the Conference. H.N. also thanks Professors Yasunori Koya and Tomohiro Sasanami for their suggestive comments and encouragement. Two anonymous reviewers, Professor Marianne V. Moore, Professor Masumi Yamamuro (The University of Tokyo), and Dr. Sachi Sri Kantha contributed helpful advice from which this manuscript greatly benefited. Mr. Akira Ooyagi (Aomori, Japan) is thanked for the generous gifts of his collected samples, especially of Drepanosurus uchidai; and Alexey I. Orgilyanov and his colleagues at the Institute of the Earth’s Crust, as well as the staff members at Limnological Institute, Siberian Branch of the Russian Academy of Sciences (Irkutsk) are also for their skilled technical assistance. This research was partly supported by the Russian Basic Research Project (0345-2019-0002): “Molecular ecology and evolution of living systems of the Central Asia in global ecological change conditions”.


  1. Alonso M, Naganawa H (2008) A new fairy shrimp Galaziella murae (Branchiopoda: Anostraca) from Mongolia. J Biol Res-Thessalon 10:119–128Google Scholar
  2. Alonso M, Ventura M (2013) A new fairy shrimp Phallocryptus tserensodnomi (Branchiopoda: Anostraca) from Mongolia. Zootaxa 3670:349–361CrossRefGoogle Scholar
  3. Belk D (1995) Uncovering the Laurasian roots of Eubranchipus. Hydrobiologia 298:241–243CrossRefGoogle Scholar
  4. Belk D, Brtek J (1995) Checklist of the Anostraca. Hydrobiologia 298:315–353CrossRefGoogle Scholar
  5. Brauer F (1877) Beiträge zur Kenntniss der Phyllopoden. Sitzungsber Kaiserl Akad Wiss Math-Naturwiss Cl Abt 1(75):583–614Google Scholar
  6. Brtek J (1966) Einige Notizen zur Taxonomie der Familie Chirocephalidae Daday 1910. Annot Zool Bot Bratislava 33:1–65Google Scholar
  7. Brtek J (1995) Some notes on the taxonomy of the family Chirocephalidae (Crustacea, Branchiopoda, Anostraca). Zbor Slov nár Múz Prír Vedy (Acta Rer Nat Mus Natl Slov Bratislava) 41:3–15Google Scholar
  8. Brtek J (1997) Checklist of the valid and invalid names of the large branchiopods (Anostraca, Notostraca, Spinicaudata and Laevicaudata) with a survey of the taxonomy of all Branchiopoda. Zbor Slov nár Múz Prír Vedy (Acta Rer Nat Mus Natl Slov Bratislava) 43:3–66Google Scholar
  9. Brtek J (2002) Taxonomical survey of the Anostraca, Notostraca, Cyclestheria, Spinicaudata and Laevicaudata. Zbor Slov nár Múz Prír Vedy (Acta Rer Nat Mus Natl Slov Bratislava) 48:49–60Google Scholar
  10. Brtek J, Mura G (2000) Revised key to families and genera of the Anostraca with notes on their geographical distribution. Crustaceana 73:1037–1088CrossRefGoogle Scholar
  11. Cottarelli V, Mura G (1975) Una nuova specie di Anostraco (Crustacea, Branchiopoda) dell’Italia Peninsulare: Chirocephalus sibyllae n. sp. Boll Zool 42:187–196CrossRefGoogle Scholar
  12. Cottarelli V, Mura G (1984) Chirocephalus ruffoi n. sp. (Crustacea, Euphyllopoda, Anostraca) di acque astatiche d’alta quota dell’Appennino Calabro-Lucano. Boll Mus civ St nat Verona 11:515–523Google Scholar
  13. Cottarelli V, Mura G, Ippolito G, Marrone F (2017) Chirocephalus sarpedonis sp. nov. (Branchiopoda, Anostraca, Chirocephalidae) from Turkey questions the monophyly of the traditional Chirocephalus species-groups. Hydrobiologia 801:5–20CrossRefGoogle Scholar
  14. Creaser EP (1930) Revision of the phyllopod genus Eubranchipus, with the description of a new species. Occ Pap Mus Zool Univ Michigan 208:1–13Google Scholar
  15. Daday (de Deés) E (1909) Novum genus et nova species Crustaceorum e subordine Phyllopoda Anostraca. Ann Mus nat Hung 7:173–174Google Scholar
  16. Daday de Deés E (1910) Monographie systématique des Phyllopodes anostracés. Ann Sci Nat Zool (9e sér) 11:91‒489Google Scholar
  17. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  18. Fischer S (1851) Branchiopoden und Entomostracen. In Middendorf AT von (ed) Reise in den äussersten Norden und Osten Sibiriens 2 (Zoologie) 1:149‒162, Buchdr K Akad Wiss, St. PetersburgGoogle Scholar
  19. Forbes SA (1876) List of Illinois Crustacea, with descriptions of new species. Bull Ill Mus Nat Hist (Bull Ill State Lab Nat Hist) 1:3–25Google Scholar
  20. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  21. Galazy GI, Naganawa H (2010) Baikal in questions and answers (Japanese edition)—11 Benthos. Aquabiology 32:468–473Google Scholar
  22. Gueriau P, Rabet N, Clément G, Lagebro L, Vannier J, Briggs DEG, Charbonnier S, Olive S, Béthoux O (2016) A 365-million-year-old freshwater community reveals morphological and ecological stasis in branchiopod crustaceans. Curr Biol 26:383–390CrossRefGoogle Scholar
  23. Hartland-Rowe R (1967) Eubranchipus intricatus n. sp., a widely distributed North American fairy-shrimp, with a note on its ecology. Can J Zool 45:663–666CrossRefGoogle Scholar
  24. Johansen F (1921) The larger freshwater Crustacea from Canada and Alaska. III. Euphyllopoda (Branchiopoda). Can Field-Nat 35:21–30Google Scholar
  25. Kikuchi H (1957) Occurrence of a new fairy shrimp, Chirocephalopsis uchidai sp. nov., from Hokkaido, Japan (Chirocephalidae, Anostraca). J Fac Sci Hokkaido Univ (ser 6) Zool 13:59–62Google Scholar
  26. Kobayashi T (1954) Fossil estherians and allied fossils. J Fac Sci Univ Tokyo (Sect 2 Geol Mineral Geogr Geophys) 9:1–192Google Scholar
  27. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  28. Linder F (1941) Contribution to the morphology and the taxonomy of the Branchiopoda Anostraca. Zool Bidrag från Uppsala 20:101–303Google Scholar
  29. Moriya H (1985) Notes on a fairy shrimp Eubranchipus uchidai (Kikuchi) (Anostraca), from Japan. Hydrobiologia 120:97–101CrossRefGoogle Scholar
  30. Murdock J (1885) Description of seven new species of Crustacea and one worm from Arctic Alaska. Proc US Natl Mus 7(1884):518–522CrossRefGoogle Scholar
  31. Naganawa H (1999) A new spinicaudatan (Crustacea: Branchiopoda) from the Island of Olkhon (Lake Baikal, Russia) and the zoogeography of East Asian Spinicaudata. Jpn J Limnol 60:585–606CrossRefGoogle Scholar
  32. Naganawa H (2001) Current classification of recent “large branchiopods”. Jpn J Limnol 62:75–86CrossRefGoogle Scholar
  33. Naganawa H, Banzragch Zagas (2003) Current prospect of the Recent large branchiopodan fauna of East Asia: 6. Revision of the genus Galaziella (Anostraca: Chirocephalidae: Galaziellinae). Aquabiology 25:387–393Google Scholar
  34. Naganawa H, Brtek J (2006) Current prospect of the Recent large branchiopodan fauna of East Asia: 9. “Living fossil” fairy shrimps, from the viewpoint of hemoglobin evolution. Aquabiology 28:527–533Google Scholar
  35. Naganawa H, Orgiljanova TI (2000) Galaziella baikalensis, a new genus and species of chirocephalid (Crustacea: Branchiopoda: Anostraca) from Russia and the zoogeography of East Asian Anostraca. Limnology 1:209–216CrossRefGoogle Scholar
  36. Naganawa H, Orgiljanova TI, Orgiljanov AI, Pisarsky BI (1996) First record of the primitive crustacean groups (Branchiopoda, Anostraca; Notostraca; Conchostraca) from the Island of Olkhon, Lake Baikal in Russia. Aquabiology 18:462–469Google Scholar
  37. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford Univ Press, New YorkGoogle Scholar
  38. Pesta O (1936) Entomostraken von der Insel Korfu (Griechenland). Zool Anz 114:241–250Google Scholar
  39. Prévost B (1803) Histoire d’un Insecte (ou d’un Crustacée) que l’auteur a cru devoir appeler Chirocéphale diaphane, et de la suite remarquable des métamorphoses qu’il subit. J Phys Chim Hist Nat Arts 57:37‒54 (also 89‒106: Suite de l’histoire d’un Insecte ou d’un Crustacée) Google Scholar
  40. Rogers DC (2013) Anostraca catalogus (Crustacea: Branchiopoda). Raffles Bull Zool 61:525–546Google Scholar
  41. Ruffo S, Vessentini G (1957) Una nuova specie di Fillopode Anostraco dei Monti Sibillini (Chirocephalus marchesonii n. sp.). Mem Mus civ St nat Verona 6:1–8Google Scholar
  42. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  43. Sars GO (1867) Histoire naturelle des Crustacés d’eau douce Norvège. Chr Johnson, ChristianiaGoogle Scholar
  44. Sars GO (1897) The Phyllopoda of the Jana-Expedition. Ann Mus Zool Acad Imp Sci St-Pétersb 2:463–493Google Scholar
  45. Sars GO (1901) On the crustacean fauna of Central Asia. Part I. Amphipoda and Phyllopoda. Ann Mus Zool Acad Imp Sci St-Pétersb 6:130–164Google Scholar
  46. Shadrin N, Anufriieva E (2012) Review of the biogeography of Artemia Leach, 1819 (Crustacea: Anostraca) in Russia. Int J Artemia Biol 2:51–61Google Scholar
  47. Simon E (1886) Étude sur les crustacés du sous-ordre des phyllopodes. Ann Soc entomol Fr (6e sér.) 6:393–460Google Scholar
  48. Steuer A (1898) [non 1899, Ján Brtek’s mistake] Die Entomostraken der Plitvicer Seen und des Blata-Sees (Croatien), gesammelt von Dr. R. Sturany (1895). Ann Hofmus Wien 13:159–188Google Scholar
  49. Takahashi N, Kitano T, Hatanaka Y, Nagahata Y, Tshistjakov YuA, Hamasaki M, Moriya H, Igarashi K, Umetsu K (2018) Three new species of the fairy shrimp Eubranchipus Verill [sic], 1870 (Branchiopoda: Anostraca) from northern Japan and far Eastern Russia. BMC Zool 3(5):1–16Google Scholar
  50. Trussova EK (1971) On the first finding of the Mesozoic species of order Anostraca (Crustacea). Paleontol Zh 4:68–73Google Scholar
  51. Trussova EK (1974) The traces of life of phyllopod crustaceans. Paleontol Sb 10:82–87Google Scholar
  52. Trussova EK (1975) On the taxonomic status of Anostraca, Crustacea from the Lower Cretaceous of the Eastern Transbaikal. Paleontol Sb 12:60–66Google Scholar
  53. Uéno M (1940) Phyllopod Crustacea of Manchoukuo. Bull Biogeogr Soc Jpn 10:87–102Google Scholar
  54. Verrill AE (1869) Contributions to zoology from the Museum of Yale College. No. III. Descriptions of some new American phyllopod Crustacea. Amer J Sci 48:244–254CrossRefGoogle Scholar
  55. Verrill AE (1870) Observations on phyllopod Crustacea of the family Branchipidae, with descriptions of some new genera and species, from America. Proc Am Assoc Adv Sci 1869B Nat Hist Zool 18:230–247Google Scholar
  56. Waloßek D (1996) Rehbachiella, der bisher älteste Branchiopode. Stapfia 42:21–28 (also Kataloge des O.Ö. Landesmuseums N.F. 100:21–28) Google Scholar
  57. Zuckerkandl E, Pauling L (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 97‒166Google Scholar

Copyright information

© The Japanese Society of Limnology 2019

Authors and Affiliations

  1. 1.Laboratory of Comparative Biochemistry, The United Graduate School of Agricultural ScienceGifu UniversityGifuJapan
  2. 2.Laboratory of Ichthyology, Limnological InstituteSiberian Branch of the Russian Academy of SciencesIrkutskRussia
  3. 3.Laboratory of Analytical and Bioorganic Chemistry, Limnological InstituteSiberian Branch of the Russian Academy of SciencesIrkutskRussia

Personalised recommendations