The Long-eared Bats of Australasia

When most people think of Australian mammals, they imagine the fauna as dominated by marsupials and monotremes, representatives of lineages long isolated from those found elsewhere. But Australia is also home to a remarkable diversity of native placentals. Immigrating from the north as Australia drifted closer to Asia, the rodents and bats underwent their own radiations on the Australian continent and its neighbouring islands. Among these distinctly Australasian assemblages of placentals are the long-eared bats or big-eared bats of the tribe Nyctophilini.

Lesser long-eared bat Nyctophilus geoffroyi, copyright Michael Pennay.

The long-eared bats comprise fifteen or so species found over a range between eastern Indonesia and Australia with outlying species in New Caledonia and Fiji. They are members of the Vespertilionidae, the most diverse recognised family of bats, and share with most other vespertilionids a fairly generalised appearance with dull coloration. They differ from other vespertilionids in having a relatively short muzzle (with a correspondingly reduced number of teeth) with a small nose-leaf at its end (Miller 1907). They also (as the vernacular name indicates) have particularly large ears, as long as or longer than the rest of the head, that are commonly connected medially by a distinct membrane. At rest, the ears may be folded like a concertina along the hind margin to protect them from damage (Hall & Woodside 1989). Historically, the long-eared bats were treated as their own subfamily within the Vespertilionidae that also included a similar North American genus Antrozous. However, the nyctophilins are now regarded as a derived tribe within the larger subfamily Vespertilioninae (albeit one whose exact relationships remain uncertain) and similarities between Nyctophilini and Antrozous are thought to be convergent rather than reflecing a close relationship. The majority of nyctophilins are placed in a single genus Nyctophilus with the exception of the New Guinea big-eared bat Pharotis imogene. This species differs from Nyctophilus in lacking hair at the end of the muzzle.

Nyctophilins are found in a range of habitats but seem to prefer dry woodlands. Vespertilionids as a whole are differentiated from other bats by modifications of the fore arms including a highly developed double joint between scapula and humerus and reduction of the ulna. As a result, they may be less powerful fliers than other bats but they would be more agile. This trend would be particularly pronounced in nyctophilins which have relatively short wings compared to other vespertilionids (Hall & Woodside 1989). The development of a nose-leaf in nyctophilins is associated with their use of signals emitted at a constant frequency through the nose for echolocation whereas other vespertilionids use signals of varying frequency emitted through the mouth. As well as catching insect prey in flight, long-eared bats are able to recognise prey at rest and so glean insects off vegetation or on the ground. This gleaning habit is presumably also associated with long-eared bats having relatively larger eyes than other vespertilionids.

Gould's long-eared bat Nyctophilus gouldi with ears partially reclined, copyright Department of Environment and Primary Industries, Victoria.

Caves in Australia are mostly not very extensive so the formation of colonies by Australian vespertilionids is constrained by the availability of suitable roosting sites such as hollows in trees or crevices in rocks. At least some long-eared bats may be solitary (Hall & Woodside 1989). Their distribution in Australia (as with pretty much all Australian animals) is also largely contingent on the availability of water. Mating happens in autumn but gestation is generally delayed, whether by delaying fertilisation or development of the embryo, and does not kick off until spring. Pregnancy then lasts about six weeks though it may again be slowed down if conditions turn bad. Long-eared bats are unusual among bats in that twins are not uncommon.

Whereas at least some nyctophilin species remain common (the lesser long-eared bat Nyctophilus geoffroyi is found over most of Australia), others are rare or little-known. A species described from Lord Howe Island, N. howensis, is believed to be extinct. The most remarkable case of obscurity is Pharotis imogene which was not recorded between 1890 and 2012, over 120 years. Evidence of extreme rarity? Quite probably, but also possibly evidence of just how few people are paying attention to bats.

REFERENCES

Hall, L. S., & D. P. Woodside. 1989. Vespertilionidae. In: D. W. Walton, & B. J. Richardson (eds) Fauna of Australia vol. 1B. Mammalia pp. 871–886. Australian Government Publishing Service: Canberra.

Miller, G. S., Jr. 1907. The families and genera of bats. Smithsonian Institution, United States National Museum, Bulletin 57: i–xvii, 1–282, pls 281–214.

Moustached Bats, Ghost-faced Bats

In the theatre of mammal diversity, there are two groups that loom above all their competitors. The most diverse of the generally recognised mammalian orders, by a healthy margin, is the rodents. Nevertheless, they are still given a good run for their money by the silver medalist, the bats. There is somewhere in the region of 1100 known living species of bat, a number that has continued to increase in recent years as study progresses. This post will focus on one particular group of bats, the Mormoopidae.

Ghost-faced bat Mormoops megalophylla, copyright Merlin Tuttle.

Mormoopids are a group of bats found in warmer parts of the Americas. They commonly go by the names of moustached bats or funnel-eared bats, at least to the extent that any type of bat can be said to 'commonly' go by anything. They are fast-flying, insectivorous bats that roost in colonies in hot, humid caves. These colonies can be sizable: at least one colony of Wagner's moustached bat Pteronotus personatus was estimated to include more than 16,000 individuals (de la Torre & Medellín 2010). In the United States, mormoopids are currently restricted to the south-west (in the form of the ghost-faced bat Mormoops megalophylla) but subfossil from Florida indicate a wider distribution in the past (Simmons & Conway 2001).

Mormoopids belong to the Noctilionoidea, a distinctly Neotropical group of bats that also includes the leaf-nosed bats of the Phyllostomidae and the Noctilio bulldog bats (and also possibly the short-tailed bat Mystacina of New Zealand, because why make things simple?) The biggest difference between mormoopids and other noctilionoids lies in the structure of their shoulders. In most bats, the trochiter (one of the tubercles at the top of the humerus) is enlarged to form a secondary articulation with the scapula. This strengthens the shoulder joint, presumably allowing the production of more power for flight. Mormoopids, however, lack this enlarged trochiter. I must confess to being unsure just what is the significance of this alteration; mormoopids remain fast fliers (de la Torre & Medellín 2010). Are they perhaps sacrificing a bit of endurance for the sake of higher mobility?

Wagner's moustached bat Pteronotus personatus, copyright Bernard Dupont.

Current classifications of the mormoopids recognise two genera in the family, Mormoops and Pteronotus. Mormoops species have a shorter head than Pteronotus species (so short, in fact, that the braincase is wider than it is long), with a markedly upturned snout. Basically, they have a skull like a pug dog. In a revision of the family, Simmons & Conway (2001) recognised two living species of Mormoops and six of Pteronotus, plus an additional species of each described from subfossil remains from Cuba. Pteronotus was also divided between three subgenera. The type subgenus included two species, Pt. davyi and Pt. gymnonotus, known as naked-backed bats because the membrane for their wings attaches close to the spine so the body fur is not visible in dorsal view (in other mormoopids, the wings attach along the sides of the body). Three of the remaining species (Pt. personatus, the sooty moustached bat Pt. quadridens and Macleay's moustached bat Pt. macleayi) were placed in a morphologically generalised subgenus Chilonycteris. The remaining living species was Parnell's moustached bat Pt. parnellii, placed in its own subgenus Phyllodia.

Pteronotus parnellii was the only known mormoopid, and in fact the only Neotropical bat of any kind, to use high duty cycle echolocation. Echolocation, of course, works through the bat emitting calls and listening for when they bounce back from surrounding objects. The problem is that the noise produced while emitting calls can drown out returning echoes. As a result, most echolocating bats use what is called low duty cycle echolocation. Individual echolocation calls are spaced apart so the bat has time between each call to listen for echoes. High duty cycle echolocation is used by two Old World bat families, the Rhinolophidae and Hipposideridae, as well as Pteronotus parnellii. These bats have learnt the trick of emitting calls continuously and recognising returning echoes by their different frequency. This allows each bat to build up a more detailed picture of its surrounds, allowing for greater mobility in complex environments such as around dense forest.

Parnell's moustached bat Pteronotus parnellii, copyright Alex Borisenko.

In recent years, however, mormoopid systematics have been given a shake-up. Many of the mormoopid species recognised by Simmons & Conway (2001) could be divided between multiple subspecies. Recently, a molecular analysis of Pteronotus species by Pavan & Marroig (2016) found strong genetic divergence between most of these subspecies. As a result, they proposed raising the distinct subspecies to species level, effectively raising the number of living Pteronotus species from six to fifteen. Some of these species could also be separated on the basis of morphometric and acoustic data; others exhibited morphometric overlap but were geographically distinct. 'Pteronotus parnellii' was the most diverse, being divided into eight named species plus an unnamed population that may warrant species recognition. The question that this immediately raises: is the use of high duty cycle echolocation a feature of all nine of these species, or might it turn out that not all members of the P. parnellii group are high duty echolocators?

REFERENCES

de la Torre, J. A., & R. A. Medellín. 2010. Pteronotus personatus (Chiroptera: Mormoopidae). Mammalian Species 42 (869): 244–250.

Pavan, A. C., & G. Marroig. 2016. Integrating multiple evidences in taxonomy: species diversity and phylogeny of mustached bats (Mormoopidae: Pteronotus). Molecular Phylogenetics and Evolution 103: 184–198. Simmons, N. B., & T. M. Conway. 2001. Phylogenetic relationships of mormoopid bats (Chiroptera: Mormoopidae) based on morphological data. Bulletin of the American Museum of Natural History 258: 1–97.

Fruit Bats in Africa

A western Woermann's fruit bat Megaloglossus azagnyi clings to the underside of a palm frond, copyright Jakob Fahr.

The diversity of bats often goes under-appreciated. With over 1200 known species around the world (with new ones continuing to be named on a regular basis), they significantly outnumber any of the other traditionally recognised orders of mammals except the rodents. The basal relationships among the bats have been subject to some disagreement in recent years but it is generally agreed that living bats can be divided between three main lineages, one of which is the Pteropodidae, the fruit bats of the Old World. Pteropodids differ in a number of ways from all other bats, the most notable of which being that they mostly do not use echolocation (some do, but not in the same way as other bats: whereas non-pteropodids use sounds produced by their vocal chords for sonar, echolocating pteropodids click with their tongues or clap their wings). Instead, pteropodids use their over-sized eyes to see their way in the dark. The most familiar pteropodids may be the large flying foxes of the genus Pteropus, but they are not the only members of the family.

Not all pteropodids are as large as the flying foxes, either. Megaloglossus is a genus of one or two species of fruit bat found in lowland rain forests in tropical Africa. They are the smallest of Africa's pteropodids (forearm length is about four centimetres, which I'm guessing translates into a wingspan of about a foot?) and differ from other African pteropodids in their slender faces and long, protrusible tongue (the latter feature, of course, explaining the genus name). For a long time, Megaloglossus was classified with other long-tongued pteropodids in a subfamily Kiodotinae, of which it would have been the only African component. However, Bergmans (1997) reclassified it as part of a uniquely African tribe, the Myonycterini, on the basis of features such as partially webbed toes and a ventral collar of thick hair. The 'kiodotines' are now recognised as a polyphyletic assemblage that have evolved their protrusible tongues convergently, presumably to feed on flower nectar.

Woermann's fruit bat Megaloglossus woermanni being handled on a stick by an interfering human, copyright Natalie Weber.

Until recently, only a single species of Megaloglossus was recognised: Woermann's fruit bat M. woermanni, originally named for a specimen from Gabon. A separate subspecies, M. woermanni prigoginei, has been suggested for larger individuals in the eastern part of the larger country now called Congo but Bergmans (1997) noted that the type specimen of the species fell within the size range for 'prigoginei'. A recent molecular study of Myonycterini by Nesi et al. (2013) identified a genetic divide between specimens from Cameroon, Gabon and the Congos on one hand and Liberia and the Côte d’Ivoire on the other, and the authors proposed recognising the latter as a separate species Megaloglossus azagnyi for which they proposed the somewhat awkward vernacular name of 'western Woermann's fruit bat'. However, M. azagnyi is recognised solely on the basis of genetic distance; no morphological distinction has yet been identified between the populations. Nesi et al. (2013) claimed that specimens of M. azagnyi were generally smaller than M. woermanni, but their reported measurement ranges indicate a broad overlap between the two. Bergmans (1997), who examined a greater number of specimens than Nesi et al., suggested a broad cline of increasing size from the west to the east of Megaloglossus' range but no definite gap. Nesi et al.'s division also leaves the status uncertain of populations in intervening regions such as Nigeria. The distribution of Megaloglossus is divided into two by the 'Dahomey gap', a region of dry coastal savannah in Benin, Togo and Ghana that splits the wetter rainforests on either side. However, as noted by Nesi et al. themselves, palaeontological records indicate that the Dahomey gap has not been consistenly present in the past, and it should not be assumed that it corresponds to the division between M. woermanni and M. azagnyi.

REFERENCES

Bergmans, W. 1997. Taxonomy and biogeography of African fruit bats (Mammalia, Megachiroptera). 5. The genera Lissonycteris Andersen, 1912, Myonycteris Matschie, 1899 and Megaloglossus Pagenstecher, 1885; general remarks and conclusions; annex: key to all species. Beaufortia 47 (2): 11–90.

Nesi, N., B. Kadjo, X. Pourrut, E. Leroy, C. P. Shongo, C. Cruaud & A. Hassanin. 2013. Molecular systematics and phylogeography of the tribe Myonycterini (Mammalia, Pteropodidae) inferred from mitochondrial and nuclear markers. Molecular Phylogenetics and Evolution 66: 126–137.

Little Yellow Bats

Specimen of an unidentified Rhogeessa, photographed by Kate Comis.
The Neotropical members of the genus Rhogeessa go by the incredibly imaginative vernacular name of 'little yellow bats'. On the face of it, this would seem to sum up the salient features of these animals pretty succinctly: they're small, they're yellow, and they're bats. Eleven species of Rhogeessa were recognised by Baird et al. (2008a), found from northern Mexico to southern Brazil. The species of Rhogeessa are rather difficult to distinguish from each other; in particular, the six species that referred by Baird et al. (2008a) to the 'Rhogeessa tumida complex' are all but indistinguishable. Nevertheless, recent authors have regarded them as good species, and it is because of the reasons why this is that the genus has attracted the most interest.

The only really reliable way to distinguish the species of the R. tumida complex is to take a look at their chromosomes. Despite their external similarity, the species have different chromosome numbers and arrangements from each other. This forms an interesting contrast to other bat genera, which may have more morphological variability but little chromosome variation. Comparison between Rhogeessa chromosomes has lead to the suggestion that the various species may have diverged as a result of a process called Robertsonian translocation.

Specimen of the Yucatan yellow bat Rhogeessa aeneus photographed by Alex Borisenko.

To explain Robertsonian translocation, I have to indulge in a bit of background terminology of chromosomes (skip this if you know all this stuff). Think of the classic picture of an X-shaped chromosome (this is actually a doubled chromosome that develops during cell division: two copies, called chromatids, have been produced of the chromosome that will be separated when the cell divides). The point where the two chromatids are joined is a region of the chromosome called the centromere: it provides an attachment point for the spindle fibres that will draw each individual chromatid apart. The centromere is not always positioned at the midpoint of the chromosome: those chromosomes in which it is are called metacentric, while other acrocentric chromosomes have the centromere close to one end so the conjoined chromatids look closer to V-shaped than X-shaped.

Translocation is a process where a piece of genetic material breaks off one chromosome and becomes attached to another. Robertsonian translocation is a particular type of translocation where two acrocentric chromosomes, by breaking at the centromeres, effectively become fused to form a single metacentric chromosome (as shown in the diagram below from here):

Robertsonian translocation has been observed in many species; it even happens occasionally in humans. Where it becomes interesting for evolutionary studies is that the resulting metacentric chromosome continues to function in the same manner as the original acrocentric chromosomes, with little or no negative effects (the short bit from each acrocentric chromosome that is lost rarely contains any functioning genes). The individual carrying the fused chromosome even remains fertile, because when meiosis occurs in any individual with both the fused and unfused chromosomes, the two unfused chromosomes will each line up with their matching arm on the fused chromosome. However, imagine a situation where one individual in a population experiences a Robertsonian translocation between two chromosomes (call them 1 and 2), but another individual has a translocation between one of those chromosomes and another chromosome (say, 2 and 3). The individual that carries chromosomes 1-2 and 3 will produce fertile offspring if mating with an unfused individual, as will that carrying 1 and 2-3. However, if the 1-2 individual mates with the 2-3, their offspring will carry both fused chromosomes. Because these chromosomes and the unfused 1 and 3 cannot easily match up in a way that allows them to be separated effectively during meiosis, the hybrid offspring will have significantly reduced fertility. This has been practically shown to be the case between Robertsonian races of mice (Capanna et al. 1977). If the two fused chromosomes each become more predominant in a population than the original unfused chromosomes (either by drift or hitchhiking), then gene flow will be slowed or stopped between individuals carrying one or the other. Hey presto, speciation!

Speciation as a result of Robertsonian translocation also provides a counter-example to those who, when objecting to the taxonomic recognition of 'cryptic' species, raise the Biological Species Concept to defend their viewpoint. Contrary to popular assumption, there is no essential correlation between speciation and morphological divergence. Even under the Biological Species Concept, two populations may be good species (i.e. non-interfertile) and yet morphologically indistinguishable.

Allen's yellow bat Rhogeessa alleni, photographed by Merlin Tuttle. Rhogeessa alleni is the most morphologically distinct species of Rhogeessa, and has been included in a separate genus or subgenus Baeodon. Baird et al. (2008a), on the basis of molecular phylogeny, recognised the subgenus Baeodon but also including R. alleni's sister species, R. gracilis.

Anyway, I have a vague memory that somewhere along the line I was talking about bats. The known karyotype numbers for Rhogeessa vary from 30 (in three species: R. alleni, R. gracilis and R. io) to 52 (in a specimen from Suriname that Baker et al. 1985 assigned to R. tumida but which almost certainly represents an undescribed species). The phylogeny for the genus that was recovered by Baird et al. (2008a, b) could be consistent with both Robertsonian fusions and fissions taking place during the genus' history. In an attempt to test whether the different karyotypes truly function as isolating mechanisms (and hence whether the chromosomal 'species' are actually species), Baird et al. (2008b) could only find genetic indicators of possible recent hybridisation between the two apparently least divergent species, R. tumida (34 chromosomes) and R. aeneus (32 chromosomes); all other species maintained reciprocal monophyly in each of the three gene types (mitochondrial, Y-chromosome and somatic chromosome) tested. Baker et al. (1985) referred to another 32-chromosome karyotype ('32N') that differed from R. aeneus (assuming, on the basis of geography, that R. aeneus corresponds to Baker et al.'s '32B') in terms of exactly which chromosomes had been fused and so would be reproductively incompatible with R. aeneus. However, this 32N form appears to be assigned by Roots & Baker (2007) to R. io, otherwise with 30 chromosomes. As 30-chromosome R. io and the 32N form differ only in a single pair fusion in the former (Baker et al. 1985), they would probably remain interfertile by the principles described earlier. In contrast, despite their apparent difference in chromosome number of only two, R. tumida and R. aeneus actually differ in five chromosome fusions (three on one side, two on the other), meaning their interfertility should be considerably lower.

And if you've gotten this far and you're still not sick of bats, Darren Naish covered Rhogeessa and its relatives as part of his mammoth series on vesper bats earlier this year.

REFERENCES

Baird, A. B., D. M. Hillis, J. C. Patton & J. W. Bickham. 2008a. Evolutionary history of the genus Rhogeessa (Chiroptera: Vespertilionidae) as revealed by mitochondrial gene sequences. Journal of Mammalogy 89 (3): 744-754.

Baird, A. B., D. M. Hillis, J. C. Patton & J. W. Bickham. 2008b. Speciation by monobrachial centric fusions: A test of the model using nuclear DNA sequences from the bat genus Rhogeessa. Molecular Phylogenetics and Evolution 50 (2): 256-267.

Baker, R. J., J. W. Bickham & M. L. Arnold. 1985. Chromosomal evolution in Rhogeessa (Chiroptera: Vespertilionidae): possible speciation by centric fusions. Evolution 39 (2): 233-243.

Capanna, E., M. V. Civitelli & M. Cristaldi. 1977. Chromosomal rearrangement, reproductive isolation and speciation in mammals. The case of Mus musculus. Bolletino di Zoologia 44 (3): 213-246.

Roots, E. H., & R. J. Baker. 2007. Rhogeessa parvula. Mammalian Species 804: 1-4.