Skip to main content
SpringerLink
Log in

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

  • Special Feature: Original Article
  • Freshwater Ecosystems - Key Problems and New Findings from Russian Lakes including Lake Baikal
  • Published:
Limnology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alonso M, Naganawa H (2008) A new fairy shrimp Galaziella murae (Branchiopoda: Anostraca) from Mongolia. J Biol Res-Thessalon 10:119–128

    Google Scholar 

  • Alonso M, Ventura M (2013) A new fairy shrimp Phallocryptus tserensodnomi (Branchiopoda: Anostraca) from Mongolia. Zootaxa 3670:349–361

    PubMed  Google Scholar 

  • Belk D (1995) Uncovering the Laurasian roots of Eubranchipus. Hydrobiologia 298:241–243

    Google Scholar 

  • Belk D, Brtek J (1995) Checklist of the Anostraca. Hydrobiologia 298:315–353

    Google Scholar 

  • Brauer F (1877) Beiträge zur Kenntniss der Phyllopoden. Sitzungsber Kaiserl Akad Wiss Math-Naturwiss Cl Abt 1(75):583–614

    Google Scholar 

  • Brtek J (1966) Einige Notizen zur Taxonomie der Familie Chirocephalidae Daday 1910. Annot Zool Bot Bratislava 33:1–65

    Google Scholar 

  • 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) 41:3–15

    Google Scholar 

  • 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) 43:3–66

    Google Scholar 

  • 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) 48:49–60

    Google Scholar 

  • Brtek J, Mura G (2000) Revised key to families and genera of the Anostraca with notes on their geographical distribution. Crustaceana 73:1037–1088

    Google Scholar 

  • Cottarelli V, Mura G (1975) Una nuova specie di Anostraco (Crustacea, Branchiopoda) dell’Italia Peninsulare: Chirocephalus sibyllae n. sp. Boll Zool 42:187–196

    Google Scholar 

  • 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 11:515–523

    Google Scholar 

  • 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 801:5–20

    Google Scholar 

  • Creaser EP (1930) Revision of the phyllopod genus Eubranchipus, with the description of a new species. Occ Pap Mus Zool Univ Michigan 208:1–13

    Google Scholar 

  • Daday (de Deés) E (1909) Novum genus et nova species Crustaceorum e subordine Phyllopoda Anostraca. Ann Mus nat Hung 7:173–174

    Google Scholar 

  • Daday de Deés E (1910) Monographie systématique des Phyllopodes anostracés. Ann Sci Nat Zool (9e sér) 11:91‒489

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    PubMed  Google Scholar 

  • 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. Petersburg

  • Forbes SA (1876) List of Illinois Crustacea, with descriptions of new species. Bull Ill Mus Nat Hist (Bull Ill State Lab Nat Hist) 1:3–25

    Google Scholar 

  • 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 3:294–299

    CAS  PubMed  Google Scholar 

  • Galazy GI, Naganawa H (2010) Baikal in questions and answers (Japanese edition)—11 Benthos. Aquabiology 32:468–473

    Google Scholar 

  • 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 26:383–390

    CAS  PubMed  Google Scholar 

  • Hartland-Rowe R (1967) Eubranchipus intricatus n. sp., a widely distributed North American fairy-shrimp, with a note on its ecology. Can J Zool 45:663–666

    Google Scholar 

  • Johansen F (1921) The larger freshwater Crustacea from Canada and Alaska. III. Euphyllopoda (Branchiopoda). Can Field-Nat 35:21–30

    Google Scholar 

  • 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 13:59–62

    Google Scholar 

  • Kobayashi T (1954) Fossil estherians and allied fossils. J Fac Sci Univ Tokyo (Sect 2 Geol Mineral Geogr Geophys) 9:1–192

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Linder F (1941) Contribution to the morphology and the taxonomy of the Branchiopoda Anostraca. Zool Bidrag från Uppsala 20:101–303

    Google Scholar 

  • Moriya H (1985) Notes on a fairy shrimp Eubranchipus uchidai (Kikuchi) (Anostraca), from Japan. Hydrobiologia 120:97–101

    Google Scholar 

  • Murdock J (1885) Description of seven new species of Crustacea and one worm from Arctic Alaska. Proc US Natl Mus 7(1884):518–522

    Google Scholar 

  • 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 60:585–606

    CAS  Google Scholar 

  • Naganawa H (2001) Current classification of recent “large branchiopods”. Jpn J Limnol 62:75–86

    CAS  Google Scholar 

  • 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 25:387–393

    Google Scholar 

  • 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 28:527–533

    Google Scholar 

  • 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 1:209–216

    Google Scholar 

  • 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 18:462–469

    Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford Univ Press, New York

    Google Scholar 

  • Pesta O (1936) Entomostraken von der Insel Korfu (Griechenland). Zool Anz 114:241–250

    Google Scholar 

  • 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)

  • Rogers DC (2013) Anostraca catalogus (Crustacea: Branchiopoda). Raffles Bull Zool 61:525–546

    Google Scholar 

  • Ruffo S, Vessentini G (1957) Una nuova specie di Fillopode Anostraco dei Monti Sibillini (Chirocephalus marchesonii n. sp.). Mem Mus civ St nat Verona 6:1–8

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sars GO (1867) Histoire naturelle des Crustacés d’eau douce Norvège. Chr Johnson, Christiania

    Google Scholar 

  • Sars GO (1897) The Phyllopoda of the Jana-Expedition. Ann Mus Zool Acad Imp Sci St-Pétersb 2:463–493

    Google Scholar 

  • Sars GO (1901) On the crustacean fauna of Central Asia. Part I. Amphipoda and Phyllopoda. Ann Mus Zool Acad Imp Sci St-Pétersb 6:130–164

    Google Scholar 

  • Shadrin N, Anufriieva E (2012) Review of the biogeography of Artemia Leach, 1819 (Crustacea: Anostraca) in Russia. Int J Artemia Biol 2:51–61

    Google Scholar 

  • Simon E (1886) Étude sur les crustacés du sous-ordre des phyllopodes. Ann Soc entomol Fr (6e sér.) 6:393–460

    Google Scholar 

  • 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 13:159–188

    Google Scholar 

  • 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):1–16

    Google Scholar 

  • Trussova EK (1971) On the first finding of the Mesozoic species of order Anostraca (Crustacea). Paleontol Zh 4:68–73

    Google Scholar 

  • Trussova EK (1974) The traces of life of phyllopod crustaceans. Paleontol Sb 10:82–87

    Google Scholar 

  • Trussova EK (1975) On the taxonomic status of Anostraca, Crustacea from the Lower Cretaceous of the Eastern Transbaikal. Paleontol Sb 12:60–66

    Google Scholar 

  • Uéno M (1940) Phyllopod Crustacea of Manchoukuo. Bull Biogeogr Soc Jpn 10:87–102

    Google Scholar 

  • Verrill AE (1869) Contributions to zoology from the Museum of Yale College. No. III. Descriptions of some new American phyllopod Crustacea. Amer J Sci 48:244–254

    Google Scholar 

  • 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 18:230–247

    Google Scholar 

  • 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 

  • 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 97‒166

    Google Scholar 

Download references

Acknowledgements

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”.

Author information

Authors and Affiliations

  1. Laboratory of Comparative Biochemistry, The United Graduate School of Agricultural Science, Gifu University, 1-1 Yanagido, Gifu, 501-1193, Japan

    Hidetoshi Naganawa & Atsushi Iwasawa

  2. Laboratory of Ichthyology, Limnological Institute, Siberian Branch of the Russian Academy of Sciences, 3 Ulan-Batorskaya Street, Irkutsk, 664033, Russia

    Hidetoshi Naganawa, Elena Yu. Naumova & Elena V. Dzyuba

  3. Laboratory of Analytical and Bioorganic Chemistry, Limnological Institute, Siberian Branch of the Russian Academy of Sciences, 3 Ulan-Batorskaya Street, Irkutsk, 664033, Russia

    Natalia N. Denikina & Ilya G. Kondratov

Authors
  1. Hidetoshi Naganawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena Yu. Naumova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalia N. Denikina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ilya G. Kondratov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elena V. Dzyuba
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Atsushi Iwasawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hidetoshi Naganawa.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Marianne V Moore.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Naganawa, H., Naumova, E.Y., Denikina, N.N. et al. Does the dispersal of fairy shrimps (Branchiopoda, Anostraca) reflect the shifting geographical distribution of freshwaters since the late Mesozoic?. Limnology 21, 25–34 (2020). https://doi.org/10.1007/s10201-019-00589-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10201-019-00589-9

Keywords

Search

Navigation