Cheiromeles+torquatus


 * Naked bulldog bat ** //Cheiromeles torquatus// Horsfield, 1824

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= 1. Introduction = "//It’s a bald bird, it’s a smelly rat - no, it’s the naked bulldog bat//." Headline from an article in The Straits Times (Singapore), 19 January 1979 The saying "beauty lies in the eye of the beholder" certainly holds true for the naked bulldog bat (//Cheiromeles torquatus//). While some may find its appearance unpleasant and strange, others (like myself) find it remarkable. Regardless of how one feels about its appearance, there is no denying it is truly a fascinating creature. Its "hairless" skin, large size and almost noxious smell make it is unlike any bat that people would usually encounter.

The naked bulldog bat is one of the only two species belonging to the genus //Cheiromeles// which consists of //Cheiromeles torquatus// and //Cheiromeles parvidens.// This genus is in the insectivorous bat family, Molossidae, also known as the free-tailed bats so named for their characteristic long tails. Found only in Southeast Asia, the naked bulldog bat is widespread in its range but its abundance differs from area to area. Like all insectivorous microbats, the naked bulldog bat is nocturnal and able to echolocate.

What's in a name?
The genus name, "//Cheiromeles//", comes from the Greek word "cheir" which means "hand." This is in reference to the bat's unusual hindfoot which "has the character and properties of a hand" as described by Horsfield (1824). "//torquatus//" comes from the Latin word "torques" which means "collar". This is in reference to the collar of long hairs at the neck region of the naked bulldog bat. Its loose, wrinkled skin and enlarged canine teeth, reminiscent of an English bulldog, along with its hairless appearance is probably where the name "naked bulldog" came from (See Figure 2-3) [4]. The naked bulldog bat is also known as: hairless bat, giant naked bat , greater naked bat. = 2. Description =
 * = [[image:bat skin rolls1.jpg width="584" height="589" align="center" caption="Figure 2. Note the wrinkled rolls of skin of the naked bulldog bat. Source: Dr Tigga Kingston, used with permission."]] ||= [[image:bat yawning.png width="587" height="589" align="center" caption="Figure 4. A naked bulldog bat yawning. Note the large canine teeth. Source: Adapted from Meristogenys69, obtained and accredited under fair use."]] ||
 * [[image:Senawicrop.jpg width="530" height="519" align="center" caption="Figure 4. A naked bulldog bat next to one of the smallest bats in the world, a small wooly bat that weighs a mere 3g. Source: Adapted from Nurul Ain Elias. Permission pending. "]] || == General description ==


 * Size and weight**
 * The naked bulldog bat is considered the largest and heaviest microbat in the world . Its weight ranges from 136-200g [4][8].

|| **Brief physical description** [3]
 * Basic measurements [4]:
 * Head-body 126.8-138mm
 * Tail 53.7-70.5 mm
 * Forearm 78.6-81.1mm
 * Tibia 33.0-35.9 mm
 * Ear 18.2-20.0 ||
 * [[image:Screen Shot 2016-11-23 at 11.44.18 pm.png width="522" height="426" align="center" caption="Figure 5. A dorsal view of the naked bulldog bat. Note the unsheathed and relatively long tail. Source: Leong et al., 2009."]]
 * The dorsal side (back) of the bat is a sooty black with occasional areas of tawny. The breast and abdomen is reddish-brown.


 * The tail is unsheathed, extending out further beyond the end of the uropatgaium which is the membrane connecting the base of the tail to the bat's hind legs (Figure 5). This is a characteristic feature of bats from the Molossidae family.


 * Small and partially concealed eyes.


 * Long cylindrical head with a conical muzzle that narrows into a nose consisting of two tubes (Figure 7).


 * Its wings are long and narrow with a sharp wing tip (Figure 6).


 * The musculature of the hindlimb is more defined and larger than other insectivorous bats . ||
 * [[image:taxo4254/Screen Shot 2016-11-24 at 1.14.08 am.png width="521" height="355" align="center" caption="Figure 7. A look at the cranial and dental features of the naked bulldog bat. Source: Leong et al., 2009."]] || **Cranial and [|dental features]**


 * The canine teeth (four largest teeth visible in Figure 7) of the naked bulldog bat are extremely prominent. The upper incisors (upper front two teeth) are also much larger and converge towards the middle. The premolars and molars have sharp raised cusps [4]


 * The dental formulae is I: 2/2, C: 1–1/1–1, PM: 1–1/2–2, M: 3–3/3–3 (I: incisor, C: canine, PM: premolar, M: molar).


 * A distinct feature of its cranium is the pronounced sagittal crest which is a ridge of bone running down the top of the skull (labelled SC in Figure 7). It indicates exceptionally strong jaw muscles [24] . ||
 * [[image:Screen Shot 2016-11-23 at 5.49.12 pm.png width="513" height="285" align="center" caption="Figure 8. The skin of naked bulldog bat looks hairless unless viewed up close. Source: Merlin Tuttle’s Bat Conservation, used with permission. "]] || == Interesting distinguishing features ==


 * "Nakedness/hairless" skin**
 * A distinguishing characteristic of the naked bulldog bat is its hairless appearance which is characteristic of the genus //Cheriomeles//.


 * However, the naked bulldog bat is not actually hairless! It is covered in short, sparse and, fine hairs which are not easily observable from a distance.


 * Long hairs can be found on the bat at two regions: around a fold of skin at the neck region of the bat (Figure 9) and on the first toe of its hindfeet (Figure 10) [5]

|| **Gular pouch/sac**
 * The reduced fur reduces wind resistance, allowing the naked bulldog bat to be more aerodynamic and fly faster . ||
 * [[image:hair at gular.png width="531" height="318" align="center" caption="Figure 9. Gular pouch of a male naked bulldog bat. Source: Leong et al., 2009."]]
 * The fold of skin at the neck of the bat is called a gular pouch/sac which contains secretory glands (Figure 9) [7] [11]


 * In males, there are two separate glands, whereas in females, there is a single, large gland (Figure 10) [4]


 * The glands secrete an oily and viscous substance that has a pungent and unpleasant odour. Authors have compared the stench to "burnt leather" and "stale socks drenched in engine oil". [4]


 * The purpose of the secretions is likely to maintain optimum condition of the skin and wing membranes of the bat [4]. ||
 * [[image:taxo4254/hindfoot.png width="528" height="345" align="center" caption="Figure 11. The hindfoot of a naked bulldog bat. Source: Leong et al., 2009."]] || **Hindfoot**
 * Horsfield (1824), who originally described this species, states that the hindfeet of the naked bulldog bat is its "chief distinguishing character" [3].


 * The first toe of the hindfoot sticks out like a thumb, allowing the naked bulldog bat to hold on to surfaces easily, making the hindfoot in some ways analogous to a hand [3].


 * The first toe is also covered by stiff, bristle-like hairs. The ends of these hairs are hooked are likely used for grooming [7]. ||
 * [[image:subaxillary pouch.png width="537" height="355" align="center" caption="Figure 12. The subaxillary pouch of a naked bulldog bat. Source: Leong et al., 2009."]] || **Subaxillary pouch**
 * On both sides of the bat, under the arm, is an subaxillary pouch. When the bat is at rest and not flying, the wings fold and are tucked into these pouches.


 * This protects the delicate wing membranes, especially when the bat is moving on all fours . ||
 * [[image:Sonogram of call.png width="535" height="471" align="center" caption="Figure 13. Sonogram of the search call of a naked bulldog bat in a clear unclutter environment. i, high frequency call; ii, low frequency call. Source: adapted from Kingston et al., 2003."]] || == Sonogram of search phase call ==
 * When bats echolocate, they produce different calls. One of these calls, the search phase call is used for navigation and search in uncluttered areas. They are the most useful call type for species identification . Learn more about echolocation in bats and in the naked bulldog bat in this section: Echolocation and Diet before returning back here!


 * The naked bulldog bat produces CF-FM (Constant frequency-Frequency Modulated) calls of long duration and low peak frequencies. [31] . However, when searching for prey, the bat alternates search phase calls with lowest frequencies at 20 and 28 kHz and with a call duration of 30 and 24ms respectively at a repetition rate of 6.3Hz [6] . ||

= 3. Distribution, status and threats =

Southeast Asia
The naked bulldog bat is found only in Southeast Asia and in the following countries: Peninsular Malaysia, southern Thailand, in Indonesia, from Sumatra to Java, and across Borneo, in Philippines only on Palawan island and, in Singapore. According to the [|IUCN Red List of Threatened Species], the conservation status of the naked bulldog bat is listed as "Least Concern". This is because it has a widespread range, and although rare and facing some major threats in some parts of its range, its decline will not be fast enough to be placed in a more threatened category [2].

Singapore
The last known confirmed roost of the naked bulldog bat in Singapore was in the Bukit Timah Nature Reserve in 2009 [4]. It is hence considered to be in low abundance and highly endangered in Singapore [18]. Over the past 20 years, they have also been sighted at Chestnut drive forest, Seletar reservoir forest, Rifle Range Drive forest and the Macritchie reservoir forest [4].

Threats
In Peninsular Malaysia and Borneo, the naked bulldog bat is hunted and eaten by some indigenous tribes [2][29]. Its roosts are also destroyed in an effort to control the species as it is believed to be an agricultural pest of rice crops despite it being insectivorous [2]. The mining of cave habitats for minerals and for swiftlets' nests also disturb roosting bats.

Habitat loss is likely to be the largest threat the naked bulldog bat is facing in Southeast Asia and in Singapore.

= 4. Ecology and Biology =

Locomotion
Different bat species have different flight styles. A bat's flight style in turn influences how it hunts for prey and the ecological niche it occupies. The flight style of a bat is determined by the aspect ratio and wing tip index. To put it simply, aspect ratio is the ratio of the width of the wing to its height while a wing tip index measures how sharp the wing tip is. Bats that have a high aspect ratio (long and narrow wings) and wing tip index are fast rapid fliers while those with a low aspect ratio (short and broad wings) fly slower but have much higher maneuverability. Bats with slow, manoeuvrable flight usually forage in more cluttered environments as compared to those fast flying species that forage over wide, open spaces.

The naked bulldog bat is capable of exceptionally fast flight. Of all insectivorous bats, it has the highest aspect ratio and wing tip index.

The naked bulldog bat is also unique in that unlike most bats, it is very agile when moving on all fours. For most bats, increased acrobatics in the air came at the cost of land maneuverability as muscles used for walking had little use in flight. However as mentioned earlier unlike other insectivorous bats that have relatively slim hindlegs, the naked bulldog bat has rather broad hindlegs and its long flexible thumb which allow it to easily grip onto trips and climb backwards and upwards despite its body weight.

media type="youtube" key="-3A83XxuLXg" width="734" height="418" align="center" Watch how easily the naked bulldog bat reverse-climbs up a tree!

Habitat and Roosts
The naked bulldog bat is gregarious which means it lives in roosts with other bats of the same species. Roosts as large as 20,000 individuals have been recorded. They roost in a variety of sites: hollow trees, caves, buildings, rock crevices, and holes in the earth [2].

Echolocation and Diet


The naked bulldog bat is an aerial-hawking insectivore which means that it forages in open spaces above forests or in clearings, catching prey in flight. It uses echolocation to detect, locate and classify prey as all insectivorous bats do by producing ultrasonic pulses of sound. There are three distinct types of calls bats use: search phase, approach and terminal/feeding buzz (Figure 15). Search phase calls are used for general navigation and searching in uncluttered areas. They have the most consistent call characteristics and hence are best used for species identification. When bats approach prey or are in a more clutter environment, they emit approach calls which are more regular. A feeding/terminal buzz occurs during prey capture or pursuit and consists of short calls that are very quickly emitted together.

When a bat call is visualised on a [|sonogram], it takes on a shape that can be used to identify the bat to species. Bat calls can be sorted into different frequency structures: Constant Frequency (CF) and Frequency Modulated (FM) or CF-FM which is a mix of both. As the name implies, CF calls look like a constant line that remains at a consistent frequency level while FM calls look like decreasing gradient varying through a range of frequencies. A CF-FM call has elements of both calls. CF calls are usually emitted by bats that forage over open, wide spaces like over canopies or water while FM calls are emitted by those that forage in cluttered environments like a forest understory. Some species, like the naked bulldog bat, are able to modulate their calls depending on the habitat they are in. Their calls become more FM like in cluttered environments as compared to an uncluttered one.

The naked bulldog bat feeds mostly on flying insects like termites, flying ants and moths [6]. Its large canines, sharp cusped molars and strong jaw muscles are also indicative that it is able to feed on larger hard-shelled insects like beetles.

= 5. Taxonomy =

Taxonavigation
The classification of the naked bulldog bat is as follows [2]
 * Kingdom || Animalia ||
 * Phylum || Chordata ||
 * Class || Mammalia ||
 * Order || Chiroptera ||
 * Suborder || Yangochiroptera ||
 * Family || Molossidae ||
 * Genus || //Cheiromeles// ||
 * Species || //Cheiromeles torquatus// ||

Original description
The naked bulldog bat and the genus it belongs, //Cheriomeles//, was originally described in 1824 by Thomas Horsfield, a physician and naturalist (Figure 11) [3]. The description was extremely detailed and was accompanied by illustrations (Figure 12).



Type Specimen
The holotype for the naked bulldog bat is found in the [|Natural History Museum (London)].

The collecting data is as follows:
 * Type locality: Indonesia
 * Sex: Male
 * Life stage: Adult
 * Occurrence ID: 17adc2f5-18ee-484e-a268-e4a5b0316bbe
 * Catalog Number: 1923.10.7.9

Phylogeny
Bats belong to the order [|Chiroptera]. This order was traditionally divided into the suborders Megachiroptera which consisted of megabats and Microchiroptera consisting of microbats (echolocating bats). However recent molecular evidence has shown that microbats are paraphyletic with bats from the family [|Rhinolophidae] being in the suborder Yinpterochiroptera with megabats and other microbat families being in Yangochiroptera.

In a study by Teeling et al. (2005), they analyzed 13.7 kb of nuclear sequence data from portions of 17 nuclear genes from representatives of all bat families and four outgroups. The phylogenetic analysis used a variety of methods that included Maximum Likelihood (ML) unconstrained bootstrap values, ML constrained bootstrap values, Bayesian (single-model posterior) and, Bayesian (partitioned model posterior). Results showed a clear support for the order to be divided into two suborders, hence showing microbats to be paraphyletic and hence for the family Molossidae in the suborder Yangochiroptera (100% bootstrap support in ML analyses; Bayesian posterior probability of 1.000). The Bayesian posterior probability for the placement of Molossidae in the superfamily Vespertillionoidea was relatively high (0.94,0.91) although bootstrap support for ML analyses was rather low. Teeling et al. (2005) noted that morphological and molecular data did conflict in this area and that the use of different molecular data resulted in differing results.



Previous relationships between genera in the family Molissidae were mostly only understood through analysis of morphological data However a recent phylogenetic study has found that previous relationships proposed on morphological data were not supported. A study by Ammerman et al (2013) conducted Bayesian and Maximum Likelihood analyses of Rag2 sequences from 64 molossid bats (from 13 genera, in total 31 species) and five outgroup taxa. Results support //Cheriomeles// as the most basal lineage in the subfamily Molissinae with a BPP of 0.99 (Figure 17) [39]. This result is particularly interesting as the genus has many unusual characteristics that is not found in other genera.



DNA barcode
Nucleotide and protein sequences for the naked bulldog bat can be found at [|The National Center for Biotechnology Information]. = 6. References = All images used in this web page are used in accordance to [|Fair Use] guidelines. If you are a creator and have an issue with your work displayed on this web page, please contact me at a0115644@u.nus.edu

Figure 1, 5, 6, 7, 9, 11, 12: Leong, T. M., Teo, S. C., & Lim, K. K. P., 2009. The naked bulldog bat, //Cheiromeles torquatus// in Singapore-past and present records, with highlights on its unique morphology (Microchiroptera: Molossidae). //Nature in Singapore//, //2//, 215-230. Figure 2: Tigga Kingston. Personal image. Permission granted. Figure 3: Adapted from [|Meristogenys69], obtained and accredited under fair use. Modifications: Screen capture of relevant section. URL: https://www.youtube.com/watch?v=-3A83XxuLXg Figure 4: Nurul Ain Elias. Permission pending. URL: http://www.functionalecology.org/view/0/summaries/LaySummariesVol29Iss11.html Figure 8: Merlin Tuttle Bat Conservation. Permission granted (bat fan). URL: https://merlintuttle.smugmug.com/Low-Resolution/Roosting/i-S4QHNcS Figure 10: Dobson, G. E., 1878. Catalogue of the Chiroptera in the Collection of the British Museum. Taylor & Francis, London. xlii + 567 pp., Pls. I–XXX. Digitized by the The New York Public Library. URL: http://digitalcollections.nypl.org/items/510d47da-68ae-a3d9-e040-e00a18064a99 Figure 13: Kingston, T., Jones, G., Akbar, Z., & Kunz, T. H., 2003. Alternation of echolocation calls in 5 species of aerial-feeding insectivorous bats from Malaysia. //Journal of Mammalogy//, //84//(1), 205-215. Figure 14: “IUCN Red List Map of //Cheiromeles torquatus//” by IUCN. URL: http://maps.iucnredlist.org/map.html?id=4601 Figure 15: Heller, K. G., 1995. Echolocation and body size in insectivorous bats: the case of the giant naked bat //Cheiromeles torquatus// (Molossidae). //Le Rhinolophe//, **11**: 27–38. Figure 16, 17: Horsfield, T., 1824. Zoological Researches in Java, and the Neighbouring Islands. Kingsbury, Parbury & Allen, London. 600 pp. + 79 pls. Digitised by Smithsonian Libraries URL: http://www.biodiversitylibrary.org/ia/zoologicalresear00hors#page/14/mode/1up Figure 18: Teeling, E. C., Springer, M. S., Madsen, O., Bates, P., O'brien, S. J., & Murphy, W. J. (2005). A molecular phylogeny for bats illuminates biogeography and the fossil record. //Science//, //307//(5709), 580-584. Figure 19: Ammerman, L. K., Brashear, W. A., & Bartlett, S. N. (2013). Further evidence for the basal divergence of Cheiromeles (Chiroptera: Molossidae). //Acta Chiropterologica//, //15//(2), 307-312