Back to the future: the proper name for red-backed voles is Clethrionomys Tilesius and not Myodes Pallas

Boris Kryštufek 1 , Alexey S. Tesakov 2 , Vladimir S. Lebedev 3 , Anna A. Bannikova 4 , Nataliya I. Abramson 5  and Georgy Shenbrot 6
  • 1 Slovenian Museum of Natural History, Prešernova 20, SI-1000 Ljubljana, Slovenia
  • 2 Laboratory of Quaternary Stratigraphy, Geological Institute RAS, Pyzhevsky lane 7, 119017 Moscow, Russia
  • 3 Zoological Museum, Moscow State University, B. Nikitskaya 6, Moscow, Russia
  • 4 Lomonosov Moscow State University, Vorobievy Gory 1/12, Moscow, Russia
  • 5 Laboratory of Molecular Systematics, Zoological Institute RAS, Universitetskaya nab.1, 199034 St. Petersburg, Russia
  • 6 Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel
Boris Kryštufek, Alexey S. Tesakov
  • Laboratory of Quaternary Stratigraphy, Geological Institute RAS, Pyzhevsky lane 7, 119017 Moscow, Russia
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, Vladimir S. Lebedev, Anna A. Bannikova, Nataliya I. Abramson
  • Laboratory of Molecular Systematics, Zoological Institute RAS, Universitetskaya nab.1, 199034 St. Petersburg, Russia
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and Georgy Shenbrot
  • Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Midreshet Ben-Gurion, Israel
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  • degruyter.comGoogle Scholar

Abstract

Two names (Clethrionomys and Myodes) are used interchangeably for red-backed voles, which is contrary to one of the fundamental principles of zoological nomenclature, that each taxon has a single and unique valid name. Fixation of Mus lemmus Linnaeus, 1758, as the type of Myodes Pallas, 1811, meets the requirements stipulated in the Article 69.1.1 of the 4th edition of the International Code of Zoological Nomenclature, and is therefore valid. Hence, the genus group name Myodes is a junior synonym of Lemmus Link, 1795, and is not available for red-backed voles. The oldest valid name for red-backed voles is Clethrionomys Tilesius, 1850, with the type species (Mus rutilus Pallas, 1779) subsequently designated by Palmer (1928).

By the mid-20th century, the nomenclature of the genus group names for Holarctic mammals had largely been set (Ellerman and Morrison-Scott 1951, Miller and Kellogg 1955). Corbet (1978) stressed the need for the stability of zoological nomenclature and pointed out changes which were unnecessary in his view. One of these changes was regarding red-backed voles, known at Corbet’s time under the generic name Clethrionomys Tilesius, 1850. A decade earlier, Kretzoi (1964) argued for the primacy of Myodes Pallas, 1811, over Clethrionomys based on the principal of priority. Kretzoi, however, ignored provisions of Article 23.b. in the 1st edition of the International Code of Zoological Nomenclature (International Commission of Zoological Nomenclature 1961). Namely, he should either prove that Myodes has been used as a senior synonym in the primary zoological literature during the last 50 years (i.e. since 1914) or referred the name to the Commission. The entire issue was left unresolved for nearly four decades until Carleton et al. (2003), Pavlinov (2003a,b, 2006) and Musser and Carleton (2005) began advocating Kretzoi’s view but without referring the case to the Commission. Currently, both names are used interchangeably for the same taxon and some ecologists (e.g. Zhigalskii 2012, Danilova 2017) started using them in combination as “Myodes (Clethrionomys)”. Such a practice is contrary to one of the fundamental principles of zoological nomenclature, that each taxon has a single and unique valid name. In this particular case, the nomenclatural inconsistency is above all problematic as red-backed voles are widespread and abundant in boreal and temperate forests throughout the Holarctics and are widely used in fundamental and applied research. These voles were, for a considerable period of time, a model group in research on small-mammal population dynamics (reviewed in Bashenina 1981, Petrusewicz 1983, Henttonen 2000) and recently attracted additional interest as reservoir hosts of Hantavirus (e.g. Olsson et al. 2005, Weber de Melo et al. 2015). In addition, red backed voles were since 2000 heavily used in other novel research topics, most notably in reconstructing the impact of glacial-interglacial climatic dynamics on temperate species and their survival in refugia (Deffontaine et al. 2005, Kotlik et al. 2006, Runck et al. 2009), and as a model in research on the evolution of metabolic rate (Labocha et al. 2004, Sadowska et al. 2009) and of life-history strategies (Mappes et al. 2008). Experts engaged in medical zoology, epidemiology, population ecology and many other biological subdisciplines frequently use zoological names, but have little time or interest in disentangling nomenclatural problems on their own. The instability of taxonomic names is perplexing to them, even more so when they perceive such changes as unnecessary. In our view, a replacement of Clethrionomys with Myodes is an example of an unnecessary and unjustified change. Subsequently, we list our arguments for the retention of Clethrionomys as a genus group name for red-backed voles.

The source of disagreement is the fixation of the type species for Myodes. Namely, Pallas (1811) did not fix the type as was common in his time. He based Myodes on 10 species group names which are now in seven different genera: Lemmus lemmus, Dicrostonyx torquatus, Lagurus lagurus, Microtus arvalis, Microtus socialis, Stenocranius gregalis, Alexandromys oeconomus and Clethrionomys rutilus; a further two names (alliarius and saxatilis) are nomina dubia. The type species was subsequently designated by Coues (1877: 239) who left no doubt regarding the taxonomic scope of Myodes as defined in his detailed taxonomic review of North American rodents: “The foregoing diagnosis, so drawn as to exclude Cuniculus [=Dicrostonyx], is based upon Mus lemmus of Linnaeus, and indicates a perfectly natural generic group of Arvicolinæ”. Tesakov et al. (2010: 85) interpreted this statement as a nomenclatural act of type fixation of Myodes. Carleton et al. (2014: 948) opposed the conclusion by Tesakov et al. (l.c.), claiming that a valid fixation was achieved by the subsequent act of Lataste (1883: 349), who explicitly designated Mus rutilus as the type species for Myodes. Such an interpretation, dating back to Kretzoi (1964), necessitated the replacement of Clethrionomys, a long established name for red-backed voles (cf. Ellerman & Morrison-Scott 1951, Corbet 1978) with Myodes, a name which was widely used for lemmings (current genera Myopus, Lemmus and Dicrostonyx) throughout the 19th century (e.g. Bonaparte 1845: 29, Carus 1868: 107) and into the early 20th century (Johnston 1903: 256, Winge 1908: 78). Myodes was in disuse after the nomenclature of European mammals was stabilized in the works of Trouessart (1910) and Miller (1912), until restored by Kretzoi (1964).

The central argument of Carleton et al. (2014) against Tesakov et al. (2010) is that “Coues (1877) nowhere used the words ‘type’ or ‘type species’ in a nomenclatural context in his treatment of Myodes”. The 4th edition of the International Code of Zoological Nomenclature (International Commission of Zoological Nomenclature 1999; hereafter the Code) specifies subsequent designation of the type species in Article 69.1.1, according to which the fixation is valid if the author used “an equivalent term” [to type or type species] and “if it is clear that author accepts it as the type species” (text in square brackets is ours). The following statement made by Coues, “The foregoing diagnosis [of Myodes] …., is based upon Mus lemmus of Linnaeus” undoubtedly qualifies as “an equivalent term” to type species. Furthermore, reading the account of Coues (1877) and knowing his earlier (Coues 1874) taxonomic list leaves no doubt that according to him, Myodes was identical to the current concept of Lemmus. One can presume with good reason that Coues (1877), who was, at any rate, not strict in quoting type species, saw no reason for the argument that Mus lemmus is the type of Myodes. Namely, his concept of “Mus lemmus of Linnaeus” as the type species for Myodes was so concordant with the practice of his time (e.g. Thomas 1896) that no further mention was needed.

We conclude that Coues’ (1877) act of fixing Mus lemmus as the type species of Myodes fulfils the stipulations of the Code and is therefore valid. Myodes is thus antedated by Lemmus Link, 1795, and as such, its junior synonym. For further arguments, see Tesakov et al. (2010). If an author established a nominal genus but did not fix its type species (as is the case with Myodes), the first author who subsequently designated one of the originally included nominal species fixed the type species for the taxon and no later designation is valid (Article 69.1. of the Code). The earliest designation of the type species for Myodes is by Coues (1877); hence the act by Lataste (1883) is predated and therefore invalid. The correct name for red-backed voles remains Clethrionomy Tilesius (Palmer 1928).

Arguments against the validity of Coue’s act of type fixation are exposed at length in Carleton et al. (2014). Their text provides an interesting insight into the development of the concept of type in the 19th century, but the discussion on how Coues understood and applied the type concept in his various publications is irrelevant from the nomenclatural point of view. Instead, the entire argument made by Carleton et al. (2014) exemplifies what Corbet (1978: 8) called the product of “zoologically sterile research into the early literature” and “a pedantic search for loopholes”. The replacement of Clethrionomys with Myodes served no meaningful zoological or nomenclatural purpose but introduced unnecessary confusion and resulted in the current use of two generic names for red-backed voles.

Because Coues made a valid designation of Mus lemmus Linneaus as the type of Myodes Pallas, the genus group name Myodes is a junior synonym of Lemmus Link and is therefore not available for red-backed voles. The oldest valid name for red-backed voles is Clethrionomys Tilesius with Mus rutilus Pallas, 1779 as the type species (subsequent designation by Palmer 1928: 87). Clethrionomys contains five extant species: Clethrionomys californicus (Merriam, 1890), Clethrionomys centralis (Miller, 1906), Clethrionomys gapperi (Vigors, 1830) (in Gapper 1830), Clethrionomys glareolus (Schreber, 1780) and Clethrionomys rutilus (Pallas, 1779).

Funding: Slovenian Research Agency (to BK), Grant Number: research core funding 493 No. P1-0255.

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    • Crossref
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    • Crossref
    • PubMed
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    • Crossref
    • Export Citation
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  • Bashenina, N.V. (ed.) 1981. Bank vole. Nauka, Moscow. pp. 351 (in Russian, title and list of contents in English).

  • Bonaparte, C.L. 1845. Catalogo metodico dei mammiferi europei. Luigi di Giacomo Pirola, Milano.

  • Carleton, M.D., G.G. Musser and I.Y. Pavlinov. 2003. Myodes Pallas, 1811, is the valid name for the genus of red-backed voles. In: (A. Averianov and N. Abramson, eds.) Systematics, phylogeny and paleontology of small mammals. Proceedings, International Conference, devoted to the 90-th anniversary of Prof. I. M. Gromov. November 24–27, 2003. Zoological Institute RAS, Sankt Petersburg. pp. 96–98.

  • Carleton, M.D., A.L. Gardner, I.Y. Pavlinov and G.G. Musser. 2014. The valid generic name for red-backed voles (Muroidea: Cricetidae: Arvicolinae): restatement of the case for Myodes Pallas, 1811. J. Mammal. 95: 943–959.

    • Crossref
    • Export Citation
  • Carus, J.V. 1868. Handbuch der Zoologie. Band 1, Wirbelthiere. Verlag Wilhelm Engelmann, Leipzig.

  • Corbet, G.B. 1978. The mammals of the Palaearctic region: a taxonomic review. British Museum (Nat. Hist.), London.

  • Coues, E. 1874. Synopsys of the Muridae of North America. Proc. Acad. Nat. Sci. Philadelphia 1874: 173–196.

  • Coues, E. 1877. Family Muridae. In: (E. Coues and J.A. Allen, eds.) Monographs of North American Rodentia. Report of United States Geological Survey of the Territories 9. Government Printing Office, Washington, D.C. pp. 1–264.

  • Danilova, L.A. 2017. The dynamics of the number of rodents in the territory of landscape and ecological provinces of the south of Tyumen region. Vestnik KrasGAU 9: 100–108 (in Russian with English abstract).

  • Deffontaine, V., R. Libois, P. Kotlik, R. Sommer, C. Nieberding, E. Paradis, J.B. Searle and J.R. Michaux. 2005. Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Mol. Ecol. 14: 1727–1739.

    • Crossref
    • PubMed
    • Export Citation
  • Ellerman, J.R. and T.C.S. Morrison-Scott. 1951. Checklist of Palaearctic and Indian mammals 1758 to 1946. Trustees of the British Museum (Nat. Hist.), London.

  • Gapper, Dr. 1830. Observations on the quadrupeds found in the district of Upper Canada extending between York and Lake Simcoe, with the view of illustrating their geographical distribution, as well as describing some species hitherto unnoticed. Zool. J. 5: 200–207.

  • Henttonen, H. 2000. Long-term dynamics of the bank vole Clethrionomys glareolus at Pallasjärvi, northern Finnish taiga. Polish J. Ecol. 48 (Suppl.): 87–96.

  • International Commission on Zoological Nomenclature. 1961. International Code for Zoological Nomenclature adopted by the XV International Congress of Zoology. International Trust for Zoological Nomenclature, London.

  • International Commission on Zoological Nomenclature. 1999. International Code for Zoological Nomenclature. Fourth edition. International Trust for Zoological Nomenclature, London.

  • Johnston, H. 1903. British mammals. An attempt to describe and illustrate the mammalian fauna of the British Islands from the commencement of the Pleistocene period down to the present day. Hutshinson & Co., London.

  • Kotlik, P., V. Deffontaines, S. Mascheretti, J. Zima, J.R. Michaux and J.B. Searle. 2006. A northern glacial refugium for bank voles (Clethrionomys glareolus). Proc. Natl. Acad. Sci. USA 103: 14860–14864.

    • Crossref
    • Export Citation
  • Kretzoi, M. 1964. Über einige homonyme und synonyme Säugetiernamen. Vert. Hung. 6: 131–138.

  • Labocha, M.K., E.T. Sadowska, K. Baliga, A.K. Semer and P. Koteja. 2004. Individual variation and repeatability of basal metabolism in the bank vole, Clethrionomys glareolus. Proc. R. Soc. Lond. B 271: 367–372.

    • Crossref
    • Export Citation
  • Lataste, F. 1883. Introduction a l’étude des campagnols de France. Historique de la classification des campagnols. Le Naturaliste: journal des échanges et des nouvelles 2: 347–349.

  • Mappes, T., M. Koivula, E. Koskela, T.A. Oksanen, T. Savolainen and B. Sinervo. 2008. Frequency and density-dependent selection on life-history strategies – a field experiment. PLoS One 3: e1687.

    • Crossref
    • PubMed
    • Export Citation
  • Merriam, C.H. 1890. Descriptions of twenty-six new species of North American mammals. North Am. Fauna 4: 1–60.

  • Miller, G.S. 1906. Some voles from the Tian Shan region. Ann. Mag. Nat. Hist. 7th ser. 17: 371–375.

    • Crossref
    • Export Citation
  • Miller, G.S. 1912. Catalogue of the mammals of western Europe (Europe exclusive of Russia) in the collection of the British Museum. British Museum, London.

  • Miller, G.S. and R. Kellogg. 1955. List of North American recent mammals. US Nat. Mus. Bull. 205: 1–954.

  • Musser, G.G. and M.D. Carleton. 2005. Superfamily Muroidae. In: (D.E. Wilson and D.M. Reeder, eds.) Mammal species of the world. A taxonomic and geographic reference. Third edition. Volume 2. John Hopkins Univ. Press, Baltimore, MD, USA.

  • Olsson, G.E., N. White, J. Hjältén and C. Ahlm. 2005. Habitat factors associated with bank voles (Clethrionomys glareolus) and concomitant hantavirus in northern Sweden. Vector-Borne Zoon. Dis. 5: 315–323.

    • Crossref
    • Export Citation
  • Pallas, P.S. 1779. Novæ species quatrupedum e glirum ordine cum illustrationibus variis complurium ex hoc ordine animalium. Academia Petropolitana, Erlangae.

  • Pallas, P.S. 1811. Zoographia Rosso-Asiatica, sistens omnium animalium in extenso Imperio Rossico et adjacentibus maribus observatorum recensionem domicilia, mores et descriptiones, anatomen atque icones plurimorum. Tomus primus. Officina Caes. Academiae Scientarium impress, Petropoli [St. Peterburg].

  • Palmer, T.S. 1928. An earlier name for the genus Evotomys. Proc. Biol. Soc. Washington 41: 87. [Quoted as having 2 pages (e.g. Carleton et al. 2014: 958; however p. 88 was left blank in the original publication].

  • Pavlinov, I.Y. 2003a. Systematics of recent mammals. Archives of the Zoological Museum of Moscow State University 46:1–287+vi pp. of Index (in Russian with English Abstract).

  • Pavlinov, I.Y. 2003b. Myodes Pallas 1811 is a valid name for the genus of red-backed voles (Cricetidae). Zoologicheskii Zhurnal 85: 667–669 (in Russian with English Abstract).

  • Petrusewicz, K. (ed.) 1983. Ecology of the bank vole. Acta Theriol. 28, Suppl. 1: 242.

  • Runck, A.M., M.D. Matocq and J.A. Cook. 2009. Historic hybridization and persistence of a novel mito-nuclear combination in red-backed voles (genus Myodes). BMC Evol. Biol. 9: 114.

    • Crossref
    • PubMed
    • Export Citation
  • Sadowska, E.T., K. Baliga-Klimczyk, M.K. Labocha and P. Koteja. 2009. Genetic correlations in a wild rodent: grass-eaters and fast-growers evolve high basal metabolic rates. Evolution 63: 1530–1539.

    • Crossref
    • Export Citation
  • Schreber, J.C.D. 1780. Die Säugethiere in Abbildungen nach der Natur mit Beschreibungen. Theil 4. Wofgang Walther, Erlangen, pp. 593–936.

  • Tesakov, A.S, V.S. Lebedev, A.A. Bannikova and N.I. Abramson. 2010. Clethrionomys Tilesius, 1850 is the valid generic name for red-backed voles and Myodes Pallas, 1811 is a junior synonym of Lemmus Link, 1795. Russ. J. Theriol. 9: 83–86.

  • Thomas, O. 1896. On the genera of rodents: an attempt to bring up to date the current arrangement of the order. Proc. Zool. Soc. Lond. 1896: 1012–1028.

  • Tilesius, W.G. 1850. Glirium species in Bavaria nonnullae. Isis 2: 27–29.

  • Trouessart, E.-L. 1910. Conspectus mammalium Europae. Faune des Mammifères d’Europe. R. Friedländer & Sohn, Berlin.

  • Weber de Melo, V., H. Sheikh Ali, J. Freise, D. Kuhnert, S. Essbauer, M. Mertens, K.M. Wanka, S. Drewes, R.G. Ulrich and G. Heckel. 2015. Spatiotemporal dynamics of Puumala hantavirus associated with its rodent host, Myodes glareolus. Evol. Appl. 8: 545–559.

    • Crossref
    • PubMed
    • Export Citation
  • Winge, H. 1908. Pattedyr. Danmarks Fauna. G.E.C. Gad, København [Copenhagen] (in Dannish).

  • Zhigalskii, O.A. 2012. Seasonal dynamics of bank vole population in Udmurtya. Vestnik Udmurtskogo Universiteta 4: 64–70 (in Russian with English Abstract).

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Mammalia is a peer-reviewed journal devoted to the inventory, analysis and interpretation of Mammalian diversity. It publishes original results on all aspects of systematics (comparative, functional and evolutionary morphology; morphometrics; phylogeny; biogeography; taxonomy and nomenclature), biology, ecology and conservation of mammals.

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