Blyth's Horseshoe BatRhinolophus lepidus (Blyth, 1844)

Frontal picture of the face of Blyth's Horseshoe bat Picture credits: Nick Baker, EcologyAsia.com

Introduction

Image of a male Blyth's Horseshoe bat in Orange morph. Notice the small eyes and complex nose structure. Picture used with permission and credit to Benjamin Lee.

Blyth's Horseshoe bat (Rhinolophus lepidus) is one of the many species of horseshoe bat belonging to the genus Rhinolophus. They acquired their name from their unique spear or leaf shaped nose structure, as well as their fur which gives off a glossy look when view from an angle. They generate their echolocation from the nasal structure (nostril) and the echos received with the nose, which differs from other insectivorous bats which utilize laryngeal echolocation. As such it is possible for the bat to feed and echolocate concurrently! Like most insectivorous bats, they have small eyes and their field of vision often limited by their noseleaf^[1] . Here is a link to an introductory video of the Blyth's Horseshoe bat by Dr Tigga Kingston from Texas Tech University.

Distribution map of the Blyth's Horsehoe bat. Image taken from IUCN

The range of R. lepidus is mainly paleotropical and widespread in Southeast Asia. It has been recorded in Afghanistan, India, Southern China, Burma, Myanmar, Thailand, Cambodia, Vietnam, Penisular Malaysia and Singapore[1] ^[2] .

They are insectivorous and their wings are adapted to give them extremely flexible flight control to hunt for insects among a clustered environment[1]. With their complex nose structure, they are able to use echolocation to help them navigate and detect objects in the environment. They do so by emitting high frequency sounds and analyzing the returning sound echo to orientate and "see" their environment^[3] . Their highly acrobatic flight along with their echolocation capabilities allow them to hunt down flying insects in mid-air with great efficiency, also known as aerial hawking. Here is a video showing them in action.

Conservation status of Blyth's Horseshoe bat. Image taken from IUCN website

According to the IUCN, R. lepidus is considered least concern in terms of vulnerability to extinction. This is likely due to their widespread distribution as well as abundance in the areas. However, they also face threats from human such as bush meat hunting and tourism souvenir trade. In recent years, more and more attention have been directed to R. lepidus and other bats due to emerging diseases in recent decades and in general, bats potential role as disease reservoirs.

Behavior and Biology

Flight morphology and locomotion

Wing of a bat showing the different sections of flight membrane. Image credit to J. Gebhard, 1982. Image taken from The Biology of Bats, by G. Neuweiler, 2000.

The wings of the bat is a modified mammalian forearm. The bones are elongated and form a supporting structure for the membrane resembling the tough and rigid frame of an umbrella^[4] ^[5] . The membrane can be divided into 4 general regions: the plagiopatagium (fifth finger to rump); the propatagium (shoulder to wrist); the chiropatagium (fifth finger to wing tip) and the uropatagium (legs to tail). The first two regions support the main bulk of the body during flight, while the third helps the bat to propel forward during flight and the last helps the bat to catch prey during mid flight.

Bats are capable of both hovering and horizontal flight. The flight style of the bat is related to the shape of the wing (aspect ratio) and the wing loading (for technical details, do refer to this useful web page). Bats that forage in open space are characterized by long and pointed wings for fast, energetically efficient flight but at the cost of reduced maneuverability; whereas bats that forage in more cluttered habitats have short and broad wings, increasing their maneuverability at the cost of slower flight and energetically expensive long distance flight[6] .

Rhinolophus lepidus have short, broad wings (low aspect ratio) and a low wing loading. This allow them to perform flights with great maneuverability and perform acrobatic turns to pursue flying insects in the foliage and hover while hunting.

Echolocation

A sonogram of the echolocation call of the Glossy Horeshoe bat. CF stands for constant frequency and FM stands for frequency modulated. The call peaks around 97khz and the bands below 97khz are harmonics. Image used with permission and credit to Benjamin P. Y-H. Lee. Annotation by Lim Zong Xian

Complex echolocation systems have evolved in the Microchiropteran bats and in some Megachiropteran bats. A bat echolocation call can consist of two frequency structures: a constant frequency (CF) structure and a frequency modulated (FM) structure. Depending on the bat species, their calls can be dominated by one of the structures or a mixture of both. In a CF structure (Narrowband), the call remains at a constant frequency level for the duration of the call and is suited for detecting the velocity of an object as well as compensating for Doppler shift in the wings of the target. Whereas for the FM structure (Broadband), the call varies through a range of frequencies by a downward sweep during the call and is adapted for highly accurate target discrimination[4] ^[6] .

Each call structure (CF, FM, CF-FM) is adapted from an acoustic environment niche and as such imposes ecological restriction for foraging bats [6]^[7] . In open uncluttered areas, bats often use long search calls with narrowband and in intervals of 2-3 wing beats. Whereas for bats foraging in highly cluttered areas, a larger bandwidth call is emitted at a higher frequency to help orientate the bat. The call structure of each bat species is shaped by their diet, habitat,flight morphology and they could vary depending on the environment[4] [6] .

Echolocation was also used for water body recognition aside from foraging. Study also suggest such habitat recognition is likely to be innate in bats^[8] . The above video (taken from Youtube channel Nature) showcase the experiment using flight cages and a variety of surfaces to test their hypothesis. This innate behavior is found in a wide variety of bats, including a closely related species of R. lepidus.

Rhinolophus lepidus echolocates using Quasi-CF calls with a peak of 97.8 khz enclosed by an initial and terminal FM downsweep[3] [4] . Their echolocation structure is suited for a cluttered environment (tree foliage), aimed at hunting flying insects at edges and gaps in the foliage by aerial hawking [4] [5] ^[9] . The CF component aids in medium range detection of prey while the short FM downsweep improves the classification and localization of the targets along with a more defined "picture" of the background (vegetation, objects)[6] .

Diet

Prey remains isolated from the feces of the Blyth's Horseshoe bat. Image credit to Ponmalar & Vanitharani, 2014.

The diet for insectivorous bats is dependent on a variety of factors such as skull and dental structure, wing morphology and echolocation behavior[4] ^[10] . The size of the skull and dental structure determines the type (hard vs soft) and size of prey. The wing morphology and behavior helps to determine the manner of foraging and the environment best suited to the bat.

Generally, bats with longer signal at lower frequencies are able to search out a wider area due to lower atmospheric attenuation whereas bats with shorter calls at higher frequency have a smaller search area. However, bats with shorter calls are more suited to detect small insects[4] .

Rhinolophus lepidus mainly prey on soft flying insects such as butterflies, moths and wasp by aerial hawking . The peak frequency call (97.8khz) of the bat allows them to prey on eared moths effectively as the call are above the hearing range of the moths (20-70khz)^[11] . However recent studies suggest that the hearing range of eared moths are wider and subjected to variation depending on geographical location^[12] ^[13] . In this case, it is likely that high frequency calls are "softer" and thus the moths can only detect the bats at a much shorter distance, reducing their response time and providing the bat with a higher chance of success[11] .

Roosting and foraging

Rhinolophus lepidus is a cave roosting species with a wide foraging range up to 11km a night^[14] . They roost in small groups of up to four bats to large colonies of around 400 bats in caves and their habit of roosting in clusters is rather unique among the Rhinolophids^[15] . They will roost wherever they can hang freely and will wrap their wings fully around their body, unlike most other bats which fold their wings at the side.

They typically hunt alone in the foliage of trees (cluttered environment) and may perch under a branch to enjoy their meal. They seem to display high fidelity to a hunting site and have been observed to hunt near man-made houses (under the porch and shelter), especially during rainy periods[15] .

Breeding

Individuals reach sexual maturity at about 2 years of age and females have a gestation period of around 7 weeks. Youngs are generally born in late spring and in a study conducted in India, clusters are found to be sexually segregated when the pups are born in early May[1] . Typical of most bats, R. lepidus is generally long-lived (6-7 years) and give birth to a single pup each time.

Significance

Ecological role

A Bat Hawk (Machaeramphus alcinus) perching on the tree. Photo credit to Mark Louis Benedict, image captured on April 28 2015. Creative commons.

A rat snake (Elaphe flavirufa) swallowing a bat caught in a cave. Image credit to Pavel Kirillov, image captured July 29 2012. Creative commons.

Rhinolophus lepidus serves the role of both predator and prey in the ecosystem. Some of the common natural predators of bats include bat hawk and vipers. These predators usually hunt for the bats during their emergence period or when they are returning to their roost[10] . Specific predators of R. lepidus and bats in general are not well documented and literature are not informative on that matter in Singapore context. However it can be assume the common predators of other species of bats prey on R. lepidus as well, such as the sighting of Crested Goshawks (link to Singapore bird group) preying on fruits bats by nature photographers in Singapore.

Every night, insectivorus bats such as R. lepidus, can consume large amount of flying insects, keeping insect population in check. Bats play an important pest control role in agriculture. Their nightly feeding frenzy helps to control the population of pest insects on agriculture crops, saving the industry across the world billions of dollars[10] .

Emerging diseases and Disease reservoir

Many animals serve as natural reservoirs for various viruses, including wild ungulates (cows and horse)^[16] , rodents^[17] and birds^[18] ^[19] . Bats, both Megachiropteran and Microchiropteran, play host to a wide variety of viruses and diseases (natural reservoir) as well. Due to their unique immune system, they rarely succumb to diseases and thus are able to carry and host the disease vectors for long periods of time ^[20]. Fortunately, such diseases rarely spread to humans because bats are rarely in contact with humans^[21] .

However, with the rise of globalization, deforestation, and increased human-wildlife interaction, many previously dormant and highly pathogenic diseases were introduced into human society due to human encroachment into wildlife territory and the bridging of the natural barrier^[22] ^[23] ^[24] . Both the Nipah virus outbreak in 1999 in Malaysia and Singapore^[25] ^[26] and the SARS-Cov outbreak in 2003^[27] ^[28] , involved bats as one of the potential reservoir hosts[20] in the transmission pathway of the disease, from wildlife to humans. The Chinese Horseshoe bat (Rhinolophus sinicus) were found to be natural reservoirs of SARS-CoV^[29] ^[30] and Nipah virus was transmitted from infected pigs to humans with the flying foxes acting as reservoirs for the virus[24] .

A hypothesis on how transmission to humans occurs involves vectors (something akin to a middleman). Some of these vectors could be arthropods such as mosquitoes and midges which feed on both the blood of bats and humans; mammals such as pigs, dogs and horses^[31] ^[32] that could possibly come into contact with the body fluids (urine, saliva, excretion) of bats with the viruses. Other hypothesis includes direct contact such as consumption of bush meat or accidental bite from handling and aerosols transmission in highly populated bat caves[21] .

Much research has been done and is ongoing with regards to the pathogenicity (ability to infect) of bat-borne virus to humans[21] . Aside from that, it is important to focus on other underlying causes of emerging diseases, such as the encroachment of human activities into previously uninhabited habitats (including bat roosts). All possible factors associated with the emergence of such infectious disease should be emphasised and evaluated so that bats do not become the sole target for persecution and extermination^[33] .

Threats

Although bats in general have been hunted for bush meat in various parts of the world, the main threat to R. lepidus populations is likely to be impact from tourism. Clearing of forest and converting natural bat habitat into tourism attractions (caves, karst structures) reduces the number of available roost and foraging grounds. In certain areas, bats may be forced to form smaller colonies due to lack of available roost, which might limit and impede their reproduction . Many bat species, including R. lepidus were caught and mounted into a glass box to be sold as a tourism merchandise.

Description and morphology

For further identification needs, here is a morphological key for the bats in Southeast Asia.

Illustration of the general anatomy of the insectivorous bat. Image taken from Boonsong and McNeely, 1988, Mammals of Thailand.

Illustration of a typical Rhinolophus face. Image taken from Boonsong and McNeely, 1988, Mammals of Thailand.

A male adult Blyth's Horseshoe bat with reddish-brown color pelage. With permission and credits to Dr. Leong Tzi Ming

A male adult Blyth's Horseshoe bat with Blackish grey color pelage. With permission and credits to Nick Baker, Ecologyasia.com

General descriptions

Dimensions [1]^[34]
- Tail: 19.9 ± 0.15 mm (Singapore); 15-20 mm (Thailand)
- Pinna: 15.8 ±0.14 mm (Singapore); 15-16 mm (Thailand)
- Forearm: 39.9 ± 0.18mm (Singapore); 37-42 mm (Thailand)
General distinguishing features
- Variable pelage (fur) colorLarge ears without tragus and with well developed antitragus
  - Reddish brown
  - Blackish grey
  - Those found in dryer habitat tend to be paler compared to those in humid areas
- Long tail connected to legs by membrane (interfemoral) with the tip free
- Wings broad with rounded tips

Illustration of Blyth's Horseshoe bat face. Image taken from Boonsong and McNeely, 1988, Mammals of Thailand.

A close up picture of the "Horseshoe" like nasal structure. Notice the shape of the sella with the illustration. Image used with permission and credit to Dr. Ian Mendenhall. Annotation by Lim Zong Xian.

Nasal structure

Horseshoe shaped- anterior leaf (the lower portion of the nose indicated by white arrow) covers the lower lips and surround the nostril
- median groove simple
The sella describes the underpart of the "pointy growth" of the nose or the connecting process (frontal view in yellow circle).
- The sella is small with no side growth (lateral process or lappets), resembling a thumb and has a wide base
A pointy connecting process between the sella and lancet (in red circle)

Skeletal and dental structure of R. lepidus. Image taken from Boonsong and McNeely, 1988, Mammals of Thailand.

Skull and Dental structure

The nasal region of the skull has a distinct expansion, resulting in a lump which the noseleaf rests against
Lower second premolar external
First and Third premolars may contact each other
Dental formula
- 1/2 1/1 2/3 3/3 x 2 = 32
Form of jaw and teeth reflects the diet of the bat[4]

Taxonomy and Phylogenetics

Kingdom	Animalia
Phylum	Chordata
Class	Mammalia
Order	Chiroptera
Suborder	Yinchiroptera
Family	Rhinolophidae
Genus	Rhinolophus
Species	Rhinolophus lepidus

Recent advances in molecular technology and techniques have allowed researchers to better understand the phylogenetics of the various bat taxa. This has resulted in better clarity of the relationships among the various taxa as well as resolving conflicts in past studies, in which higher classification of Chiroptera were complicated by the use of different data set across studies. Molecular techniques used in recent studies have also uncovered important evidences to suggest that many traditionally categorized groups are no longer monophyletic^[35] .

The Family Rhinolophidae and genus Rhinolophus

In a recent study conducted by Teeling et al. in 2000^[36] , the authors challenged the concept of microbat monophyly. Their study conducted a phylogenetic analysis of bat relationships with the use of four nuclear genes and three mitochondrial genes. From the results, the authors proposed that the superfamily Rhinolophoidea (in which Rhinolophidae is part of) are closer in relationship to the megabats than to other microbats. This subsequently implied that complex echolocation in bats could have evolved twice, independently in the rhinolophids and other microbats or echolocation was lost during the evolution of megabats. A link to the article can be found here.

Phylogenetic tree from Bayesian analyses and posterior probabilities value, using CytB gene. Image taken and credit to Agnarsson et al. 2011.

A calibrated phylogeny of bat families with divergence time analysis. The years scale in million years and the grey bars represent 95% confidence interval. Image taken and credit to Agnarsson et al. 2011.

A study conducted by Agnarsson et al. in 2011^[37] uses CytB (mitochondrial gene marker) to approximate the species-phylogeny of the Chiroptera and to constructe a genealogy tree for 50% of bat taxa. The Rhinolophidae were considered a sister family with the Hipposideridae, which is also supported by previous studies^[38] ^[39] ^[40] . Rhinolophidae is supported as a monophylectic group in the full analysis of the study. Rhinolophus lepidus is clustered with R. sinicus and R. thornasi with good support from the Bayesian analysis. With regards to the geographical origin of the Rhinolophidae, there are different conclusions based on different studies. Studies that sort the Rhinolophidae by morphological analyses concluded that they are of Asian origin whereas studies utilizing molecular analysis arrived at the conclusion of a European origin.

The divergence analysis shows that the Rhinolophidae diverged with the Hipposideridae 36.9 million years ago (m.y.a), which is supported and estimated from the age of their fossil^[41] . The divergence time analysis shows the split of the Oriental clade (representative Rhinolophus affinis) and African clade (representative Rhinolophus blasii) to be roughly 11.4 m.y.a.

Rhinolophus Lacépéde, 1799, is a taxon exclusive to the Old world[42] . They are distinguished from other clades due to the fusion of various bones (manubrium, first 2 ribs, last cervical and 2 thoracic vertebrae) to form a solid pectoral ring which allow them to echolocate without moving. The phylogenetics are rather poorly resolved with many deviance in the trees with different techniques used.

Phylogenetic tree with Bayesian posterior probabilities (value above node) and Parsimony bootstrap (value below node). African region (node N) and Oriental region (node G). Image taken from Stoffberg et al. 2010. Permission pending.

Pruned Bayesian topology used in DIVA and MULTIDIVTIME analyses in Stoffberg et al. 2010. Letter above line= continents (A,Africa; B, Europe; C, Asia; D, Australia). Letter below line= zoogeographical regions (A, African; B, Palaearctic; C, Oriental; D, Australasian). Image taken from Stoffberg et al. 2010. Permission pending.

A study by Stoffberg et al. in 2010 [41] managed to establish a more robust phylogenetic relationship of the clades within Rhinolophus by geography. Traditionally, most studies conducted their molecular analysis with the use of a single gene CytB, showing weak bootstrap support (<70) for some of the clades and some node relationship is uncertain. In the study, CytB was used along three other DNA intron to form a data matrix that was comparatively successful at elucidating the evolutionary relationship. The study was able to find strong evidence to support two geographical clades for the Rhinolophus : African and Oriental groups. They also concluded that they diverged approximately 35 million years ago and they arose in Asia before radiating into Europe and Africa. Rhinolophus lepidus is clustered with R. pusillus and R. monoceros with good support by both Bayesian probability and parsimony bootstrap, indicating close relationship among the three species. The tree also indicate the Asian/Oriental ancestry of the R. lepidus.

The species Rhinolophus lepidus

Rhinolophus lepidus was first described by Blyth in 1844 (Blyth, 1844). The type specimen used by Blyth was obtained from India, Bengal, Calcutta. A holotype is currently stored at Natural History Museum London.

Holotype for Rhinolophus lepidus
GBIF ID: 1056419048
Catalog no.: 1879.11.21.151
Other catalog no.: NHMUK (ecatalogue: 4284943)
Sex/stage: Male Adult
Properties: Both wet and dry (skull) samples
Locality: India

Subspecies

Rhinolophus lepdius cuneatus K. Andersen, 1918
Rhinolophus lepidus feae K. Andersen, 1907
Rhinolophus lepidus monticola K. Andersen, 1905
Rhinolophus lepidus refulgens K. Andersen, 1905

There have been many studies on the limit and recognition of the subspecies. Rhinolophus shortridgei was initially considered and published as a subspecies as Rhinolophus lepidus shortridgei based on traits such as skull, mandible and hind foot length. However upon investigation of the type skull along with specimens from the other subspecies, the naming was resolved and R. shortridgei is considered a full species[35] .

Etymology

Eytmology of the name Rhinolophus lepidus was obtained from the Online Etymology Dictionary. Loosely translated, it means charming or fine nose, which aptly describes the nose of R. lepidus!

Glossary

Noseleaf - A form of complex nasal structure present in bats from Rhinolophidae, Phyllostomidae and Megadermatidae
Echolocation - A method for animals to recognize objects in their environment by emitting calls and listening to the echos
Pelage - Fur, hair or wool of a mammal
Tragus - A small pointed protuberance on the external ear, usually partially covering the ear canal
Aerial hawking - A form of hunting by aerial predators, prey pursued and caught in flight
Paleotropical - A zoogeographical region comprising of Africa, tropical Asia, New Guinea and many Pacific island
Sonogram - A graph representing a sound, showing the distribution of energy at different frequencies
Megachiroptera - Suborder of Chiroptera, consist of the fruit bats in general
Microchiroptera - Suborder of Chiroptera, consist of the echolocating bats
Insectivorous - A diet consisting mainly of insects and invertebrates
Frugivorous - A diet consisting mainly of fruits or preferred to fruits
Fidelity - Adherence
Gestation - Period of development inside the womb between conception and birth
Emerging diseases - Infectious diseases that has appeared in a population for the first time or previously existed but is rapidly spreading in cases or geographical range.
Disease reservoirs - Long term host of a pathogen of an infectious disease
Karst structures - structures formed from the dissolution of soluble rocks such as limestone. Characterized by sink-holes and caves
Bush meat - wildmeat, meat from non-domesticated animals

Resources

Morphological keys/ Identification guides for bats

A key to the bats of South Asia
- http://threatenedtaxa.org/ZooPrintJournal/2010/July/o235205vii101001-1076.pdf
- http://threatenedtaxa.org/ZooPrintJournal/2010/July5/Srini_bat_key.htm
Field guide to Amazonian Bats
- http://www.merlintuttle.com/2016/09/16/field-guide-amazonian-bats/

Books

The Biology of bats by Gerhard Neuweiler, 2000
Bats of Krau Wildlife Reserve by Tigga et al., 2006
Mammals of Thailand by Boonsong and McNeely, 1988
Ecology, evolution, and behaviour of bats: The proceedings of a symposium held by the Zoological Society of London and the Mammal Society: London, 26th and 27th November 1993

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