As a European person, I find European voles (and, to a degree, Asian voles) pretty familiar, commonplace, homely. Still interesting, mind you. But when it comes to North American voles --- oh my god, the weird. I don’t even know where to start, so I’ll just launch right in and hope that the crazy string of words that I see forming in front of me as I write this article will make some sort of sense, and won’t give you a seizure or anything like that.

So, the western USA – Oregon and California – is home to the tree voles: the three Arborimus species. Long-haired, dark- or reddish-brown and generally short-faced and cuddly in appearance, tree voles are specialised climbers, moving proficiently on branches and trunks with slow, deliberate movements that make them very different from most other small rodents. The idea that there might be arboreal voles is not that radical – after all, tree-climbing and tree-dwelling are all over the place within muroid rodents – but what’s especially odd about Arborimus is that it’s only the females that live in trees; males (while capable of climbing) live in subterranean burrows or in piles of vegetation. In order to meet up with females (who might be 30 m up in the trees), the males do of course climb, and they also build nests in trees during the mating season (this lasts from February to September). Nevertheless, it seems that we have a fundamental difference here in how males and females partition the habitat. Is this reflected in their morphology? I don’t know, and I don’t know if anyone else knows: comparatively little is known about Arborimus and it was “long considered difficult to find and was unusual in museum collections” (Nowak 1999, p. 1465).

I know that North America is a big place, and that it doesn’t have quite the same length of scientific tradition that Europe does, but, still, the idea that continental mammal species like this might be so poorly known remains surprising. Having said that, there are European mammals known from a handful of specimens – do people realise how little we actually know about so many animals?

What sort of vole is Arborimus? I’m not sure on that since I haven’t seen any phylogenetic studies that incorporate it. However, here we have to talk about the heather voles, since several authors have regarded Arborimus as part of another North American vole taxon*: Phenacomys, otherwise containing the Western P. intermedius and Eastern or Ungava heather voles P. ungava (these two were regarded as conspecific until recently. A few subspecies have been recognised for P. ungava but their validity is questionable). Heather voles occur across much of Canada and also across the higher regions of the Rockies, Sierra Nevadas and around the Great Lakes (McAllister & Hoffman 1988). Fossils show that they were far more widespread across the USA during the Pleistocene.

* It has also been suggested that one of the three tree voles, A. albipes, should be included within the otherwise fossil taxon Paraphenacomys.

Heather voles were long thought to be rare but, since the 1950s, they’ve become known from an increasing number of localities and specimens and the Western heather vole even seems to be increasing its range in some areas, perhaps because logging practices are providing the more open habitat that it prefer. In fact, “a variety of conflicting observations on the rarity of [these voles] have been made” (Clark & Stormberg 1987, p. 164). There are some indications that they're harder to trap than is usual for voles (McAllister & Hoffman 1988). Population explosions of the sort known for severeal voles sometimes occur. Overgrazing of suitable habitat seems to be a cause of concern for these species.

What do heather voles look like? They’re a bit boring, being highly similar to the myriad Microtus and Myodes/Clethrionomys species that make up the bulk of vole diversity. They aren’t reddish dorsally like Myodes/Clethrionomys voles and have greyer, fluffier fur than other voles in their range. They’re unlike Microtus voles in having closed roots on the cheek teeth. Their teeth are hypsodont, however, and are also distinctive in being quite obviously asymmetrical when seen in occlusal view – the lingual triangles are much larger than the buccal ones. These features (and other dental ones) are also seen in the fossil Blancan vole Hibbardomys, so it might be a close relative (Martin 2007), both being included within the clade Phenacomyini.

There are differing views on where these voles fit in phylogenetic terms. Martin (2007) regarded phenacomyines as nested within the same clade as Microtus and Myodes/Clethrionomys, whereas molecular studies have supported the arguably more interesting possibility that, together with Dicrostonyx (the collared lemmings), heather voles belong outside the clade that includes the vast majority of other voles (Conroy & Cook 1999, Cook et al. 2004, Galewski et al. 2006). According to this latter hypothesis, heather voles and collared lemmings are perhaps as distinct from microtine voles and kin as are true lemmings (Lemmus) and perhaps muskrats (Ondatra). Shock horror: radical stuff. I suppose I don’t really need to say that several additional phylogenetic hypotheses have been published for voles and lemmings (see also Chaline & Graf 1988 and Chaline et al. 1999).

Fact: muskrats are voles, and what is Dinaromys?

Incidentally, the idea that muskrats are voles is pretty awesome. Consider that an ‘average’ vole is less than 10 cm long and weighs somewhere between 20 and 50 g. Now consider the Muskrat Ondatra zibethicus: a vole with a total length of more than 60 cm (head + body length = 22-32 cm) and which can weigh up to 1.8 kg. So, it would take almost 40 ‘average’ voles to make up one muskrat. Muskrats – ondatrines – have an extensive fossil history extending back into the Miocene.

As just mentioned, muskrats might be outside the clade that contains virtually all other voles, but they might not be: muskrats are part of the same clade as water voles (Arvicola) and red-backed voles (Clethrionomys or Myodes) in some topologies (Galewski et al. 2006). Conroy & Cook (1999) found a muskrat + Arvicola clade to be the sister-group to remaining voles as well as lemmings.

By the way, the weird and poorly known Balkan snow vole or Martino’s vole Dinaromys bogdanovi is an ondatrine according to some rodent workers. A miniature, terrestrial muskrat that lives in the mountains of south-eastern Europe? Err, wow. There are other views on the affinities of this taxon, however: Chaline et al. (1999) say that it should be included within the fossil taxon Dolomys of the European Pliocene and Pleistocene, a close relative (according to them) of the also fossil Pliocene-Pleistocene Pliomys. And that's a whole 'nother story...

Colour-change ‘lemmings’ with bi-pronged seasonal super-claws

I mentioned Dicrostonyx – the collared lemmings or varying lemmings, the several species of which occur across the far north of Scandinavia, Asia and North America. Well, don’t get me started on them. First of all, these stocky, short-tailed muroids – denizens of the treeless tundra and definitely cold-adapted – look extremely lemmingy, and hence are conventionally regarded as close relatives of the ‘other’ lemmings (Lemmus, Synaptomys and Myopus) and classified with them within Lemmini, an arvicolid group supposedly distinct from the vole clade. Lemmings proper might still be a clade (Conray & Cook 1999, Cook et al. 2004), but it now seems that collared lemmings aren’t among them. Seeing as there’s no push (so far as I know) to get them renamed ‘collared voles’, the term ‘lemming’ is currently applied to unrelated short-tailed, cold-adapted arvicolids.

Secondly, unlike several other vole taxa living in modern North America, collared lemmings are not invaders from the Old World. Seemingly, they're ancestrally North American animals that invaded Asia and Europe from a Beringian centre of origin. I say this based on the presence in Pleistocene Alaska of Predicrostonyx hopkinsi, sometimes called Hopkins’s lemming and supposed to be ancestral to Dicrostonyx. Thirdly, they’re anatomically odd: they seasonally change colour from greyish or brownish to white – they are totally unique among rodents in this respect – and also grow incredible enlarged, double-pronged manual claws* on the 3rd and 4th fingers during the winter too. These claws (or, technically, claw sheaths) are shed during the summer. Their pinnae are strongly reduced: essentially just being a slim semicircle of tissue concealed by pelage.

* Some sources describe these as "cornifications of the toepads", which suggests that they're not claw sheaths per se. This isn't correct: they are claw sheaths. The pads on the 3rd and 4th fingers become enlarged at the same time as the bifid claws develop. Baby collared lemmings born in the winter have these bifid claws (Hansen 1957). Studies show that their development is hormonally controlled and linked to photoperiod (e.g., Mallory et al. 1981).

There are a few things I’d like to know here and I don’t. What are the underlying bony unguals like? Would we ever guess from their anatomy that they support enlarged, double-pronged sheaths? And are there special adaptations that enable the ‘winter claws’ to become detached? And, given that we have a group of rodents here where the unguals support two highly distinct sorts of claw sheaths at different stages of the animal’s life, here’s another cautionary tale for inferring horny claw shape from fossils (where, typically, only the bony ungual is preserved).

And that’s where we have to end for now. There’s other stuff I’d like to say about voles: I’ll get to it eventually. Rodents for the win.

One final thing. Getting good, usable images of the rodents discussed here is hard, so I had to generate images of my own. To make them prettier, I asked Gareth Monger for help: Gareth previously helped out with my Platyhystrix, and is better known for his pterosaur illustrations. Gareth has a facebook page here. Thanks loads to him for his hard work.

For previous Tet Zoo rodent articles, see…

Refs - -

Chaline, J., Brunet-Lecomte, P., Montuire, S., Viriot, L. & Courant, F. 1999. Anatomy of the arvicoline radiation (Rodentia): palaeogeographical, palaeoeocological history and evolutionary data. Annales Zoologici Fennici 36, 239-267.

- . & Graf, J. D. 1988. Phylogeny of the Arvicolidae (Rodentia): biochemical and paleontological evidence. Journal of Mammalogy 69, 22-33.

Clark, T. W. & Stormberg, M. R. 1987. Mammals in Wyoming. University of Kansas, Museum of Natural History.

Cook, J. A., Runck, A. M. & Conroy, C. J. 2004. Historical biogeography at the crossroads of the northern continents: molecular phylogenetics of red-backed voles (Rodentia: Arvicolinae). Molecular Phylogenetics and Evolution 30, 767-777.

Conroy, C. J. & Cook, J. A. 1999. MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. Journal of Mammalian Evolution 6, 221-245.

Galewski, T., Tilak, M.-K., Sanchez, S., Chevret, P., Paradis, E. & Douzery, E. J. P. 2006. The evolutionary radiation of Arvicolinae rodents (voles and lemmings): relative contribution of nuclear and mitochondrial DNA phylogenies. BMC Evolutionary Biology 2006 6: 80 doi:10.1186/1471-2148-6-80

Hansen, R. M. 1957. Development of young varying lemmings (Dicrostonyx). Arctic 10, 105-117.

Mallory, F. F., Elliott, J. R. & Brooks, R. J, 1981. Changes in body size in fluctuating populations of the collared lemming: age and photoperiod influences. Canadian Journal of Zoology 59, 174-182.

Martin, R. A. 2007. Arvicolidae. In Janis, C. M., Gunnell, G. F. & Uhen, M. D. (eds) Evolution of Tertiary Mammals of North America, Vol. 2. Cambridge University Press, Cambridge, pp. 480-497.

McAllister, J. A. & Hoffman, R. S. 1988. Phenacomys intermedius. Mammalian Species 305, 1-8.

Merriam, C. H. 1889. Description of a new genus (Phenacomys) and four species of Arvicolinae. North American Fauna 2, 27-45.

Nowak, R. M. 1999. Walker’s Mammals of the World, Volume II (Sixth Edition). The John Hopkins University Press, Baltimore and London.