Time to continue our trek across the vesper bat cladogram. In the previous article we looked at the bent-winged bats (or miniopterids, or miniopterines): a highly distinctive, morphologically novel group that seem to have diverged from vesper bats proper something like 45 million years ago. Their distinctive nature and long history of isolation relative to other lineages conventionally included within Vespertilionidae mean that bent-winged bats are now argued by many to be worthy of 'family' status. As we'll see here, they're no longer unique - bat workers now argue that another lineage of weird, highly divergent bats should also be separated from Vespertilionidae, and also raised to 'family' status [composite below shows - l to r - Cistugo lesueuri, Kerivoula pellucida and Murina suilla].

The Cistugo bats

Prior to the 1990s, most authors regarded the weird Cistugo bats from southern Africa as closely related to, or even part of, the mouse-eared bat group (Myotis). Often known as wing-gland bats for the obvious reason (the function of the wing glands remains unknown so far as I can tell), the two Cistugo species also differ from Myotis bats in having particularly small anterior premolars and in having a large cusp on the fourth lower premolar. One of those curiously interesting little facts is that the type specimen of one of the two species (C. lesueuri) was killed by a housecat. Photos of these animals are few and far between: the photos below - showing a male C. seabrae, with wing gland emphasised - are Â© E. C. J. Seamark and T. C. Kearney and come from Seamark & Kearney (2006). I've tried contacting these authors about use of the photos, but none of the various email addresses online seem to work.

Since the early 1900s it's been known that Cistugo differs from Myotis in possessing those wing glands and in tooth morphology, and the taxon was originally named as a genus on account of its morphological pecularities (Thomas 1912). A different chromosome count (2n = 50, rather than 2n = 44 for Myotis) later confirmed the distinction of the taxon and led Rautenbach et al. (1993) to suggest that Cistugo might be one of the 'most basal' members of the whole vesper bat radiation. Bickham et al. (2004), Stadelmann et al. (2004) and Lack et al. (2010) seemingly confirmed this, finding wing-gland bats to fall outside the clade that included all other vesper bat taxa. Stadelmann et al. (2004) even noted how "it is even possible that these two species actually share closer phylogenetic relationships with other families of bats" (p. 185). Lack et al. (2010) suggested that Cistugo should be given its own 'family' within Vespertilionoidea: Cistugidae. The recognition of this additional lineages means that I've now modified the vesper bat cladogram - see below. The strong external similarity that the Cistugo bats have with the Myotis species either represents a plesiomorphic similarity, or strong convergence.

The kerivoulines or woolly bats

With bent-winged bats and the Cistugo bats out of the way, we now get to those lineages still universally included within Vespertilionidae sensu stricto: specifically the kerivoulines ('subfamily' Kerivoulinae) and murinines ('subfamily' Murininae. Be careful not to write it Murinae: that's the rodent clade that includes rats and mice). As explained in the vesper bat family tree article, recent phylogenetic efforts indicate that these two groups are sister-taxa. To my knowledge, the kerivouline + murinine clade doesn't have a name, but it needs one as it's consistently recovered and looks robust.

Traditionally separated from other vesper bats in their own 'subfamily' are the 20 or so woolly bats or painted bats (Kerivoula) and the four funnel-eared bats (Phoniscus) [adjacent Kerivoula illustration Â© Jonathan Kingdon, from Kingdon (1997)]. They occur across sub-Saharan Africa, Asia and Australasia. Many kerivouline species have long been known from very few specimens, and have also proved difficult to find in field studies. It seems that this is (in part) due to their good ability to avoid mist nests (Francis et al. 2007). Improved recent capture techniques have greatly improved our knowledge of woolly bat distribution and systematics and three species have been described since 2004 (K. kachinensis Bates et al., 2004, K. titania Bates et al., 2007 and K. krauensis Francis et al., 2007).

As suggested by their common name, woolly bats have a woolly pelt, the hairs of which tend to have a crinkled appearance and frosted coloration. The pelt ranges from brownish to greyish, with some species having shiny grey tufts of fur, superficially resembling clumps of moss and hence perhaps assisting with camouflage. Several species have brightly coloured patches on their wing membranes or pelt. In the Painted bat K. picta [shown below; photo courtesy of Ismor Fischer] the membranes are both orange and black, while in K. argentata the body is black and orange, with white tips to the hairs. As usual with brightly coloured or strikingly patterned bats, these species are thought to derive improved camouflage from this pigmentation: K. picta has been reported to roost among dry leaves and flowers. At least some species (I'm thinking of the Clear-winged woolly bat K. pellucida) have a "glandular diamond-shaped swelling ... on the fourth vertebra of the tail" (Bumrungsi et al. 2006, p. 350).

In both Kerivoula and Phoniscus species, the cranium is strongly domed (but most of this is concealed by fur), the muzzle is fairly long and pointed (compared to that of other vesper bats), and the ears are large, pointed and funnel-shaped. In the funnel-eared bat P. atrox, deep grooves run along the outside of its canines (Francis et al. 2007) and it's sometimes known as the Groove-toothed bat. So it's yet another mammal showing that grooved canines do not necessarily correlate with venomosity (so far as we know).

Low aspect ratio wings, low wing loading and large tail membranes indicate high manoeuvrability and slow flight in cluttered habitats; at least some species (like the Golden-tipped bat P. papuensis of Australia, New Guinea and the Biak-Supiori Islands) appear to be spider specialists, presumably 'hover-gleaning' and picking spiders off their webs (Schulz 2000).

Molecular clock estimates suggest that these bats originated in the Late Oligocene or Early Miocene and that most speciation events within Kerivoula occurred in the Pliocene or Pleistocene. These diversification events were perhaps driven by the expansion and contraction of forest habitat that occurred across the Sunda shelf region across this time (Anwarali Khan et al. 2010). One woolly bat species, K. africana, has been suggested to be extinct, but only because it's only ever been known from a single specimen (collected in Tanzania in 1878). The Miocene African bat Chamtwaria has been regarded as a close relative of Kerivoula.

Vesper bats with tubular nostrils: Murina and Harpiocephalus

Another large vesper bat genus (it contains about 23 species) from this region of the tree is Murina, commonly termed the tube-nosed bats [adjacent photo shows M. suilla from Thailand, from Bumrungsi et al. (2006)]. As indicated by the name, the most notable thing about these bats is that their nostrils emerge at the ends of short fleshy tubes. Nasal tubes like this are more usually associated with megabats where they're present in the fruit bats Nyctimene and Paranyctimene (and short tubes are also present in Cynopterus). However, the Murina species aren't unique, as the closely related Harpiocephalus species also have such structures. Hairy-tailed bats (Lasiurus) and the Proboscis bat Rhynchonycteris naso (an emballonurid) also have soft-tissue nostril extensions of some sort. It's been proposed that tube-nosed fruit bats possess these tubular nostrils as they help keep the nostrils away from the mushy fruit consumed by these bats (Peterson 1966), but this can hardly apply to the insectivorous vesper and emballonurid bats. It seems that Murina bats eat insects and spiders, apparently gleaning them from leaves while using a slow, fluttering flight.

Murina species occur across Asia, from southern Siberia to Indonesia and the Philippines, and in New Guinea and northern Australia as well. They have a thick, woolly pelt and range in fur colour from golden yellow through reddish and brownish to grey. Unsurprisingly for a group whose distribution centres across south-east Asia, a large number of new species have been described in the last few years from Vietnam, Cambodia and Taiwan; in fact, the number of recognised species has about doubled since the start of the century. Several Murina species are extremely poorly known: M. tenebrosa from Tsuschima Tsushima Island (Japan) and M. grisea from northern India, for example, are known only from their holotypes. The adjacent image (from Csorba et al. (2007)) shows the skulls of (top to bottom) M. tiensa from Vietnam, M. harrisoni from Cambodia, M. huttoni from India, and M. rozendaali from Malaysia.

The one or two Harpiocephalus bat species - sometimes called hairy-winged bats - inhabit tropical Asia and are said to prefer hilly, forested country. 'They' (read on) have thick, woolly fur like the tube-nosed Murina bats but differ from them in having more massive, blunter-cusped teeth. This seems to match with the fact that stomach contents have included beetle remains (Nowak 1999). While it's generally hypothesised that Murina and Harpiocephalus are sister-taxa, Agnarsson et al. (2011) found their one sampled Harpiocephalus species (labelled as H. mordax) to be nested within Murina. Also of interest is that these authors found a bat conventionally included within Myotis (M. cf. nipalensis kukunorensis) to be part of the kerivouline + murinine clade. This might be a mistake but deserves further study.

The validity of H. mordax is controversial. Apparently, all the specimens ever discovered are female. Matveev (2005) argued that H. mordax is most likely synonymous with the only other currently recognised Harpiocephalus species, H. harpia (and some previous authors had regarded H. mordax as one of several H. harpia subspecies anyway). Circumstantial support for this view comes from a case where, in handled specimens of H. harpia, the smaller male was preliminarily identified as H. harpia while the larger female was identified as H. mordax (Matveev 2005). Females are not only bigger in these bats, they also have a proportionally longer rostrum, enlarged incisors and canines and a bigger sagittal crest. Incidentally, sexual dimorphism is common in vesper bats, with females typically being larger (Myers 1978). Most hypotheses invoked to explain this point to the advantages that pregnant or baby-carrying females might gain from their larger size, but there are other hypotheses too. The H. harpia shown here is from Matveev (2005).

The name 'hairy-winged bat' isn't especially helpful, by the way. Many bats possess at least some fur on their wing membranes, so the term 'hairy-winged bat' has been applied to various, distantly related and otherwise dissimilar species. It's perhaps best associated with the noctules, in particular with Leisler's bat Nyctalus leisleri. So, 'Hairy-winged tube-nosed bats' works better for the Harpiocephalus species.

With bent-winged bats, Cistugo bats, and both kerivoulines and murinines out of the way, we'll start looking at vespertilionine vesper bats next. We begin with the large, widely distributed Myotis bats.

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

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

Refs - -

Agnarsson, I., Zambrana-Torrelio, C. M., Flores-Saldana, N. P. & May-Collado, L. J. 2011. A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS Currents 011 February 4; 3: RRN1212. doi: 10.1371/currents.RRN1212.

Anwarali Khan, F. A., Solari, S., Swier, V. J., Larsen, P. A., Abdullah, M. T. & Baker, R. J. 2010. Systematics of Malaysian woolly bats (Vespertilionidae: Kerivoula) inferred from mitochondrial, nuclear, karyotypic, and morphological data. Journal of Mammalogy 91, 1058-1072.

Bickham, J. W., Patton, J. C., Schlitter, D. A., Rautenbach, I. L. & Honeycutt, R. L. 2004. Molecular phylogenetics, karyotypic diversity, and partition of the genus Myotis (Chiroptera: Vespertilionidae). Molecular Phylogenetics and Evolution 33, 333-338.

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.

Csorba, G., Thong, V. D., Bates, P. J. J. & Furey, N. M. 2007. Description of a new species of Murina from Vietnam (Chiroptera: Vespertilionidae: Murininae). Occasional Papers, Museum of Texas Tech University 268, 1-9.

Francis, C. M., Kingston, T. & Zubaid, A. 2007. A new species of Kerivoula (Chiroptera: Vespertilionidae) from Peninsular Malaysia. Acta Chiropterologica 9, 1-12.

Kingdon, J. 1997. The Kingdon Field Guide to African Mammals. Academic Press, San Diego.

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

Matveev, V. A. 2005. Checklist of Cambodian bats (Chiroptera), with new records and remarks on taxonomy. Russian Journal of Theriology 4, 43-62.

Myers, P. 1978. Sexual dimorphism in size of vespertilionid bats. The American Naturalist 112, 701-711.

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

Peterson, R. 1966. Silently, by Night: About the Little-Known but Fascinating World of Bats. Longman, London.

Rautenbach, I. L., Bronner, G. N. & Schlitter, D. A. 1993. Karyotypic data and attendant systematic implications for the bats of southern Africa. Koedoe 36, 87-104.

Schulz, M. 2000. Diet and foraging behaviour of the golden-tipped bat, Kerivoula papuensis: a spider specialist? Journal of Mammalogy 81, 948-957.

Seamark, E. C. J. & Kearney, T. C. 2006. New distribution of the Angolan wing-gland bat (Cistugo seabrae Thomas, 1912). African Bat Conservation News 7, 2-4.

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

Thomas, O. 1912. A new vespertilionine bat from Angola. Annals and Magazine of Natural History (Series 8) 10, 204-206.