Pipat Soisook

How and Why Overcome the Impediments to Resolution: Lessons from rhinolophid and hipposiderid Bats

Abstract The phylogenetic and taxonomic relationships among the Old World leaf-nosed bats (Hipposideridae) and the closely related horseshoe bats (Rhinolophidae) remain unresolved. In this study, we generated a novel approximately 10-kb molecular data set of 19 nuclear exon and intron gene fragments for 40 bat species to elucidate the phylogenetic relationships within the families Rhinolophidae and Hipposideridae. We estimated divergence times and explored potential reasons for any incongruent phylogenetic signal. We demonstrated the effects of outlier taxa and genes on phylogenetic reconstructions and compared the relative performance of intron and exon data to resolve phylogenetic relationships. Phylogenetic analyses produced a well-resolved phylogeny, supporting the familial status of Hipposideridae and demonstrated the paraphyly of the largest genus, Hipposideros. A fossil-calibrated timetree and biogeographical analyses estimated that Rhinolophidae and Hipposideridae diverged in Africa during the Eocene approximately 42 Ma. The phylogram, the timetree, and a unique retrotransposon insertion supported the elevation of the subtribe Rhinonycterina to family level and which is diagnosed herein. Comparative analysis of diversification rates showed that the speciose genera Rhinolophus and Hipposideros underwent diversification during the Mid-Miocene Climatic Optimum. The intron versus exon analyses demonstrated the improved nodal support provided by introns for our optimal tree, an important finding for large-scale phylogenomic studies, which typically rely on exon data alone. With the recent outbreak of Middle East respiratory syndrome, caused by a novel coronavirus, the study of these species is urgent as they are considered the natural reservoir for emergent severe acute respiratory syndrome (SARS)-like coronaviruses. It has been shown that host phylogeny is the primary factor that determines a virus’s persistence, replicative ability, and can act as a predictor of new emerging disease. Therefore, this newly resolved phylogeny can be used to direct future assessments of viral diversity and to elucidate the origin and development of SARS-like coronaviruses in mammals.

A taxonomic review of Rhinolophus stheno and R. malayanus (Chiroptera: Rhinolophidae) from continental Southeast Asia: an evaluation of echolocation call frequency in discriminating between cryptic species

Abstract The taxon Rhinolophus microglobosus is elevated to specific rank on the basis of clearly defined morphometric and acoustic characters which differentiate it from Rhinolophus stheno. It is recorded from Cambodia for the first time. Rhinolophus malayanus exhibits considerable geographical variation in echolocation calls, with apparently two phonic types: a northern population with lower frequency calls and a predominantly southern population with higher frequencies. However, this acoustic divergence is not reflected in any morphometric divergence, and the taxonomic status of the two phonic populations remains unclear. Discriminating characters of all three species are given, together with distribution data and short ecological summaries. The value of echolocation as an indicator of cryptic species and the zoogeographical implications of the study are briefly discussed.

A Taxonomic Review of the Hipposideros bicolor Species Complex and H. pomona (Chiroptera: Hipposideridae) in Thailand

Following extensive field work in Thailand (2006–2008), this paper reviews the taxonomic status of the three species of the Hipposideros bicolor group. Based on morphometric characters and acoustic data, the two phonic types, H. bicolor (131 kHz) and H. bicolor (142 kHz) are treated as distinct species. Hipposideros bicolor (131 kHz) is designated as H. bicolor; H. bicolor (142 kHz) is provisionally designated as H. atrox. The morphometric characters, acoustic data, and geographical distribution of H. pomona are also reviewed. The diagnostic characters of these frequently confused taxa are discussed, with a detailed study of the external, cranio-dental, and bacular morphology, and acoustic features. New data on the conservation status, distribution and ecology of these three species are included.

Echolocation call analysis and presence-only modelling as conservation monitoring tools for rhinolophoid bats in Thailand

Bats are an important component of biodiversity in Southeast Asia, and are key indicators of habitat quality. Acoustic analysis of echolocation calls not only allows the identification of bat species that are difficult to capture, but also allows for rapid and standardised ways to survey and monitor bats over large areas. However keys based on call parameters must also account for geographic variation in call parameters, and consider any effects of morphology and sex on call frequency. Presence-only modelling can predict likely geographic locations of specific taxa, and can used to refine decision making so that species unlikely to occur in a specific region can be omitted from more localised acoustic libraries. Here we develop an acoustic library for the echolocation calls of rhinolophoid bats in Thailand, and use presence-only modelling (Maxent) to explore how species with similar calls in a library developed at the national level can sometimes be largely allopatric, and hence identifiable, once geographic range is predicted. Presence-only modelling can also be used to explore whether species with similar calls adjust call frequency in likely areas of sympatry. We analysed calls from fourteen species of rhinolophid and twelve hipposiderid species from Thailand. Calls from a further three rhinolophid and one hipposiderid species are also described but not analysed statistically because of small sample sizes. Even without considering geographic variation, 69% of rhinolophid (14 species with a minimum of five individuals/ species) and 91% of hipposiderid calls (12 species) could be classified successfully to species using two call parameters (frequency of most energy (FMAXE) and duration) in a discriminant function analysis. Most of the discrimination was achieved because species often utilised different frequency bands. Morphology can also affect call frequency both across and within species. In both rhinolophids and hipposiderid families there was a negative relationship between FMAXE and forearm length. Within species, FMAXE was negatively related to forearm length in Rhinolophus microglobosus, R. pusillus and R. thomasi, and positively related to forearm length in R. affinis and R. pearsonii. Male R. pusillus called at higher frequencies than females, although there was no sexual size dimorphism in forearm length. Call frequency was negatively related to relative humidity in R. pusillus, suggesting that bats called at lower frequencies in humid environments to counter increases in atmospheric attenuation. Presence-only modelling was used to show that some species with similar call frequencies (e.g., R. lepidus and R. microglobosus; R. yunanensis and R. trifoliatus are predicted to occur largely in allopatry, and so could be identified reliably in particular parts of the country. Presenceonly modeling can assist in predicting areas of overlap between species with similar call frequencies. Other species (e.g., R. malayanus, R. coelophyllus) overlap in frequency when data from all of Thailand are combined, but seem to avoid call overlap when syntopic. Hence acoustic identification can be improved by taking into account local distribution patterns and patterns of species coexistence. The creation of call libraries at a local scale would have extensive potential as a resource to monitor changes in species distributions through time.

A review of the Murina cyclotis complex (Chiroptera: Vespertilionidae) with descriptions of a new species and subspecies

Until recently, the taxon Murina cyclotis was considered to be a widespread species, albeit one that exhibited considerable individual, sexual and geographical variation. Subsequently however, it was recognised that this taxon was in fact a complex of species. As such, in 2012, two larger forms were recognised as separate and distinct species, namely: M. peninsularis in the Sunda region and M. fionae in Laos and Vietnam. In the current paper, a new cryptic species of the cyclotis-complex is described from peninsular Thailand based on a combination of external, craniodental and genetic differences. In addition, the population previously referred to M. cyclotis from the Nicobar Islands is described as a new subspecies of this new species. Despite this work and the research of others, the taxonomy of M. cyclotis still requires further study. The description of M. peninsularis is emended and the extensive variation in its morphological characters is addressed. The diagnostic characters of each taxon, as well as the additional data on ecology, zoogeography, distribution, echolocation and genetics, where available, are summarised and discussed.

First records of Kerivoula kachinensis (Chiroptera: Vespertilionidae) from Cambodia, Lao PDR and Thailand

ABSTRACT Kerivoula kachinensis is reported for the first time from Cambodia, Lao PDR and Thailand. In April, 2005 and January, 2006, three individuals were collected in deciduous dipterocarp forest, near bamboo, in the Seima Biodiversity Conservation Area, Mondul Kiri Province, Cambodia. In September, 2007, two individuals were collected in lower montane forest, which included some mixed deciduous forest, bamboo groves and banana trees, in the hills of Phu Suan Sai National Park, Loei Province, and a single individual was collected in mixed deciduous forest, near bamboo, in the Nam Nao National Park, Petchabun Province, Thailand. In 1996–1998, seven specimens were collected from five localities in north, central and southern Lao PDR; most were associated with evergreen forest at altitudes between 150–800 m a.s.l. The species appears to be relatively widespread in continental Southeast Asia. Locally common, it is probably not currently at risk.

Morphology, genetics and echolocation calls of the genus Kerivoula (Chiroptera: Vespertilionidae: Kerivoulinae) in Thailand

Abstract Following extensive field work in Thailand (2010–2013) and the examination of 155 museum specimens, this paper reviews and examines the taxonomy of the genus Kerivoula in Thailand, based on morphology, genetics, and echolocation call characteristics. Seven species (as currently understood), Kerivoula papillosa, K. kachinensis, K. hardwickii, K. titania, K. pellucida, K. krauensis and K. minuta, were analysed in detail. Thai specimens of two species, K. picta and K. whiteheadi, were not available for study. Morphological data suggested a complex pattern of possible cryptic species, with at least five morphotypes, based on cranial data for K. papillosa, and nine for K. hardwickii, as currently understood. An analysis of the mitochondrial DNA (COI) from Thai specimens identified three genetic lineages in K. papillosa and K. hardwickii, respectively. The echolocation calls data differed significantly, albeit with individual acoustic parameters overlapping considerably, among genetic lineages. The taxonomic status of the various lineages and morphotypes are discussed.

Using Echolocation Calls to Identify Thai Bat Species: Vespertilionidae, Emballonuridae, Nycteridae and Megadermatidae

Variation in the acoustic structure of bat echolocation calls can often provide sufficient information for reliable and efficient species identification. The aim of this study was to investigate the use of echolocation call structure to identify a number of bats in the families Vespertilionidae, Emballonuridae, Nycteridae and Megadermatidae from Thailand. These species typically emit echolocation calls with a frequency-modulated (FM) sweep dominating part or all of their calls. A total of 510 echolocation calls from free-flying individuals were recorded throughout Thailand. According to the frequency-time spectra, these calls were categorized into four types: broadband FM (eight species), narrowband FM (seven species), long multiharmonic (four species) and short multiharmonic (three species). Discriminant function analysis was used to classify calls from individual bats to species. Correct classification levels were 85.9% for individuals emitting broadband FM calls (six species with adequate sample sizes), 70.4% for narrowband FM bats (seven species), 84.4% for species emitting long multiharmonic calls (four species) and 96.7% for species emitting short multiharmonic calls (two species with adequate sample sizes). However, classification rates were often low at the species level. Acoustic identification of bats emitting FM calls should be approached with caution in species-rich communities, in contrast with the identification of rhinolophoid bats where many species use distinctive constant frequencies that can facilitate identification, and provides a basis for rapid acoustic surveys of large areas in Thailand, and potentially other parts of Southeast Asia.

Description of a New Species of theRhinolophus trifoliatus-Group (Chiroptera: Rhinolophidae) from Southeast Asia

A new species of woolly horseshoe bat in the Rhinolophus trifoliatus species group is described from Sabah in Malaysian Borneo. Two specimens from Central and West Kalimantan, Indonesia are referred to this species. A fourth specimen from western Thailand is referable to this species but on the basis of ~10% genetic divergence at the cytochrome oxidase-I gene is described as a separate subspecies. Morphologically and acoustically the two subspecies are similar. With a forearm length of 52.90–54.70 mm, a skull length of 24.27–26.57 mm and a call frequency of 49.2–50.0 kHz, the new species overlaps in size and call frequency with the sympatric R. trifoliatus. However, it differs significantly in having a dark noseleaf and a uniformly dark brown pelage, resembling, but being intermediate in size between R. sedulus and R. luctus, which have a skull length of 18.99–20.17 and 26.35–32.07 mm, respectively. It also differs from R. trifoliatus in the shape and size of the rostral inflation. It can be distinguished from R. beddomei (forearm length 55.00–63.44 mm) and R. formosae (forearm length 53.85–62.40 mm), which are endemic to the Indian Subcontinent and Taiwan, respectively, by its relatively smaller body size. Acoustic and genetic data are included in the comparison between the species. Both character states support the conclusions based on morphology. Further surveys in intact evergreen forest together with a re-examination of museum specimens may reveal that this species is widespread in Southeast Asia.

A New Species of Small Hipposideros (Chiroptera: Hipposideridae) from Myanmar and a Revaluation of the Taxon H. nicobarulae Miller, 1902 from the Nicobar Islands

The taxon Hipposideros nicobarulae is elevated to a distinct species and an amended description is included. It is geographically restricted to the Nicobar Islands in the Andaman Sea where it has been found roosting in caves and deserted buildings. It is differentiated by size and external, cranial and dental morphology from Hipposideros ater from the Indian Subcontinent. Both taxa are distinguished from a new species, Hipposideros sp. nov., herein described from the Rakhine coast of western Myanmar, with referred material from Tanintharyi Division in southern Myanmar. In all cases, individuals were found roosting in human habitation. Information on the conservation status, distribution and ecology of the three species are included.