The many, many mouse-eared bats, aka little brown bats, aka Myotis bats (vesper bats part V)

One of the largest and most successful vesper bat clades is Myotis, the little brown bats or mouse-eared bats. As you can see from the simplified cladogram shown right down at the bottom of this article, recent work indicates that they form the sister-taxon to the remaining vespertilionine vesper bats (for more discussion of their phylogenetic position, see the vesper bat cladogram article). Myotis occurs virtually worldwide in diverse habitats, contains about 100 species, and has been described as the most widespread mammalian genus after Homo* [composite below shows - clockwise from far left - sleeping Bechstein's bat M. bechsteinii, Nepalese whiskered bat M. muricola, Geoffroy's bat M. emarginatus, Long-legged myotis M. volans and Greater mouse-eared bat M. myotis. All images from wikipedia].

* What about Mus?

If you don't know much about this spectacularly successful and important clade, now is the time to learn...

Many of the species within Myotis - examples include Daubenton's bat M. daubentoni [shown below, photo by Gilles San Martin, from wikipedia] in Eurasia and the Little brown bat M. lucifugus in North America - are familiar to bat-watchers of Europe, northern Africa and North America. But species within the group also occur across Asia to Javi, Bali, Borneo, the Philippines and Sulawesi, throughout Africa, in Australia (M. macropus), across the Caribbean, and in South America as far south as Patagonia. The majority of species (about 55) are Eurasian; about 24 occur in the Nearctic region, six in Africa and just three in Australasia (and the remainder are mostly Neotropical).

At least two species (M. milleri and M. planiceps, both from Mexico) seem to have become extinct in recent decades (UPDATE: see comments. The former might not be a species [but a 'subspecies'] while the latter was rediscovered in 2004). The Bocharic myotis M. bucharensis of Uzbekistan and Tajikistan (and perhaps from the adjacent countries too) hasn't been seen since the 1950s - despite expeditions in the 1970s and 80s organised specificially to find it - and might also be extinct. Recent field surveys have also failed to discover specimens of the Singapore endemic M. oreias, so it might be globally extinct as well (Pottie et al. 2005).

Myotis bats do tend to look a bit samey, though there's a range in size from a minimum of just 2.3-2.6 g for the Himalayan whiskered bat M. siligorensis to a high of 45 g for the relatively enormous Greater mouse-eared bat M. myotis. As is also the case with the bent-winged bats, woolly bats and tube-nosed bats, these bats tend to have a bulbous cranium that's much taller than the snout. The eyes appear small and are often partly obscured by fur and the ears are typically slender, about long enough to reach the snout's tip, and usually with rounded tips. A few species have unusually long ears (Bechstein's bat being a good example), or ears with a distinctive bend part way along their length (this is typical for Natterer's bat M. nattereri). Most species have brown fur of the sort typical for bats, but some are brightly coloured. The remarkable M. formosus and M. hermani from south-east Asia [the latter shown here, from Bumrungsi et al. (2006)] have lots of pink on their wing and tail membranes, and their pelage, faces and ears are mostly orange.

Mouse-eared bats tend to have low wing loading. Some species have high-aspect wings and are slow-flying hawkers in open habitats while others have relatively broad wings and are expert gleaners, sometimes relying on prey-generated noises [image below shows the North American Grey bat M. grisescens, from wikipedia]. Natterer's bat is well known for its ability to grab spiders from their webs. Several species forage over water, plucking insects and even small fish from the surface. Indeed a few species have proportionally large feet with relatively huge, strongly curved claws and seem to be specialised piscivores. The foot claws of some species - most notably the Fishing bat M. vivesi - are extremely impressive or totally ridiculous, depending on your opinion. In case you didn't know, this bat (unique to the coasts of the Gulf of California) fishes at sea - a pretty incredible bit of behaviour that has led some biologists to describe it as an honorary marine mammal. In at least one case (that of Rickett's big-footed bat M. ricketii from China, Laos and India), this distinctive foot morphology led to the prediction of piscivory prior to its proper documentation by way of scat analysis (Ma et al. 2003).

Incidentally, there is some dispute over the gender of the generic name. Myotis is said by some to be feminine; if this is followed, all the species names need to be feminine too (Nowak 1999). This isn't universally followed, with many authors still using masculine forms for some or all species. I don't know who to believe, so have simply copied the names as seen in the sources I consulted.

The quest for clades in Myotis: morphology fail?

As is often the case with enormous genera that house tens of species, authors have sought to group the various species into clusters termed subgenera. Six have generally been recognised (Nowak 1999): Myotis of Eurasia, north Africa and North America, Chrysopteron of Asia and Africa, Selysius of Eurasia and Australasia, Isotus of Eurasia and northern Africa, Leuconoe of Asia and the Americas, and Pizonyx (for M. vivesi) of North America.

However, these morphology-based clusters have not been recovered as monophyletic in recent molecular analyses (Ruedi & Mayer 2001, Hoofer & Van Den Bussche 2003, Stadelmann et al. 2004a, b, 2007): instead, the species group into clades that better confirm to biogeography. It now seems that the morphological characters previously used to unite the species within the traditional 'subgenera' arose convergently.

The distinctive Asian species M. latirostris appears to be the 'most divergent' lineage within Myotis, forming the sister-taxon to the rest of the assemblage (Stadelmann et al. 2007, Lack et al. 2010). Compared to other Myotis bats, M. latirostris is particularly small and with a strangely flattened cranium. It also differs from the others in that its lower molars are nyctalodont rather than myotodont molar structure. Stadelmann et al. (2007) suggested its morphological and molecular distinction suggested that "it should be given generic rank" (p. 45).

Among the remaining species, molecular phylogenies recover five distinct clades within Myotis (Stadelmann et al. 2004a, b, 2007): (1) a mostly American clade (consisting of separate North American and mostly South American clades) that forms the sister-group to the remainder of Myotis, (2) an all-African clade, (3) an Old World clade that includes M. macropus and M. horsfieldii, (4) an Old World clade that includes M. daubentoni and M. bechsteinii, and (5) a clade of large, Old World species that includes M. schaubi and M. myotis. The phylogenies indicate that continental exchanges have been limited for this group of bats. In view of the revised phylogeny, Hoofer & Van Den Bussche (2003) and Stadelmann et al. (2007) have suggested that it might be most appropriate to name just two of these clades (regarded either as genera or subgenera): the New World clade would be Aeorestes Fitzinger, 1870, and the more inclusive Old World clade would be Myotis proper. I'll continue to refer to the American clade as, well, 'the American clade' from hereon. [The adjacent photo shows either a Silver-tipped myotis M. albescens or Riparian myotis M. riparius (both are members of the South American clade), photographed in Brazil and kindly provided by Guilherme Siniciato Terra Garbino].

Molecular dating indicates that Myotis diverged from other vesper bats about 16 Ma ago (in the Middle Miocene) and that the American clade diverged from the rest of Myotis about 12 Ma ago (late in the Middle Miocene) (Stadelmann et al. 2004a, 2007) [the diagram above - from Stadelmann et al. (2004a) - shows a cytochrome b-based phylogeny for Myotis plotted against time. In order of divergence, from oldest to youngest, the shaded blocks correspond to clades 1-5 discussed above]. Within the American clade, it's estimated that the South American clade diverged during the Late Miocene, in which case these bats colonised the continent before the formation of the Panamanian Isthmus. Later, some members of the South American clade also dispersed over-water to give rise to the island-dwelling M. dominicensis and M. martiniquensis. The African clade diverged from the remaining Eurasian clade late in the Middle Miocene.

Poor at performing in the tropics?

While Myotis bats have successfully invaded the tropics, the diversity of tropical species is low compared to that of the northern continents. Only about ten species are endemic to the continental Neotropical region south of Panama, and only six are present in Africa. One explanation that's been put forward for this is that these bats haven't had enough time to diversify much (La Val 1973), but this is contradicted by the fact that at least some of the tropical clades are actually fairly old: as we've just seen, they've been in both the South American and African tropics since the Late Miocene. Younger vesper bat clades have managed to produce larger species clusters within shorter spans of time.

Another explanation is that these tropical Myotis bats were invading regions already densely packed with other vesper bat lineages, and were hence unable to diversify significantly (Stadelmann et al. 2007). Yet another explanation is that Myotis bats are (thanks to their Northern Hemisphere, temperate ancestry) relatively poor competitors in tropical habitats, and unable to diversify much because of their pre-adaptation to temperate climes (La Val 1973). Of course, it's also possible that tropical Myotis diversity was historically higher and just remains unsampled due to extinction and a poor fossil record.

A list of poorly known fossil bats have been regarded as close relatives of Myotis, including Stehlinia from the Eocene and Oligocene of Europe, Oligomyotis from the Oligocene of North America, and Suaptenos and Miomyotis from the Lower Miocene of North America. Hanakia from Lower Miocene Europe is sometimes said to be Myotis-like (on the basis of its three lower premolars) but has molar tooth characters more reminiscent of serotines (Rossina et al. 2006).

With this article done, we've now gotten through all the vesper bats near the 'base' of the cladogram: the miniopterids, cistugids, murinines, kerivoulines and myotines, all of which are outside the largest and most diverse vesper bat clade - Vespertilioninae. From hereon, it's all about the vespertilionines. We'll be starting with long-eared bats. Come back soon.

For previous Tet Zoo articles in the vesper bats series, see...

• Introducing the second largest mammalian 'family': vesper bats, or vespertilionids
• The vesper bat family tree: of myotines, plecotins, antrozoins, and all those cryptic species (vesper bats part II)
• Bent-winged bats: wide ranges, very weird wings (vesper bats part III)
• Of southern African wing-gland bats, woolly bats, and the ones with tubular nostrils (vesper bats part IV)

And for previous Tet Zoo articles on bats, see...

• Desmodontines: the amazing vampire bats
• Giant extinct vampire bats: bane of the Pleistocene megafauna
• Camazotz and the age of vampires
• Dark origins: the mysterious evolution of blood-feeding in bats
• A new hypothesis on the evolution of blood-feeding: food source duality involving nectarivory. Catchy, no?
• Oh no, not another giant predatory flightless bat from the future
• The most terrestrial of bats
• I stroked a pipistrelle
• Red bats
• We flightless primates
• Big animalivorous microbats
• Hidden in plain sight: discovering cryptic vesper bats in the European biota
• PROTOBATS: visualising the earliest stages of bat evolution

Refs - -

Bumrungsri, S., Harrison, D. L., Satasook, C., Prajukjitr, A., Thong-Aree, S. & Bates, P. J. J. 2006. A review of bat research in Thailand with eight new species records for the country. Acta Chiropterologica 8, 325-359.

Hoofer, S. R. & Van Den Bussche, R. A. 2003. Molecular phylogenetics of the chiropteran family Vespertilionidae. Acta Chiropterologica 5, 1-63.

Lack, J. B., Roehrs, Z. P., Stanley, C. E., JR., Ruedi, M. & Van Den Bussche, R. A. 2010. Molecular phylogenetics of Myotis indicate familial-level divergence for the genus Cistugo (Chiroptera). Journal of Mammalogy 91, 976-992.

La Val, R. K. 1973. A revision of the Neotropical bats of the genus Myotis. Sciences Bulletin, Natural History Museum of Los Angeles County 15, 1-54.

Ma, J., Jones, G., Zhang, S., Shen, J., Metzner, W., Zhang, L., & Liang, B. (2003). Dietary analysis confirms that Rickett's big-footed bat (Myotis ricketti) is a piscivore Journal of Zoology, 261 (3), 245-248 DOI: 10.1017/S095283690300414X

Nowak, R. M. 1999. Walker's Mammals of the World, Sixth Edition. The Johns Hopkins University Press, Baltimore and London.

Pottie, S. A., Lane, D. J. W., Kingston, T. & Lee, B. P. Y.-H. 2005. The microchiropteran bat fauna of Singapore. Acta Chiropterologica 7, 237-247.

Rossina, V. V., Kruskop, S. V., Tesakov, A. S. & Titov, V. V. 2006. The first record of Late Miocene bat from European Russia. Acta Zoologica Cracoviensia 49, 125-133.

Ruedi, M. & Mayer, F. 2001. Molecular systematics of bats of the genus Myotis (Vespertilionidae) suggests deterministic ecomorphological convergences. Molecular Phylogenetics and Evolution 21, 436-448.

Stadelmann, B., Jacobs, D. S., Schoeman, C. & Ruedi, M. 2004a. Phylogeny of African Myotis bats (Chiroptera, Vespertilionidae) inferred from cytochrome b sequences. Acta Chiropterologica 6, 177-192.

- ., Herrera, L. G., Arroyo-Cabrales, J., Flores-Martinez, J. J., May, B. P., Ruedi, M. 2004b. Molecular systematics of the fishing bat Myotis (Pizonyx) vivesi. Journal of Mammalogy 85, 133-139.

- ., Lin, L.-K., Kunz, T. H. & Ruedi, M. 2007. Molecular phylogeny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. Molecular Phylogenetics and Evolution 43, 32-48.