Journal of Threatened Taxa | www.threatenedtaxa.org | 26 July 2016 | 8(7): 8953–8969
Bats (Mammalia: Chiroptera) of the southeastern Truong Son Mountains, Quang Ngai Province, Vietnam
Nguyen Truong Son 1, Thomas J. O’Shea 2, Jeffery A. Gore 3, Csorba Gabor 4, Vuong Tan Tu 5, Tatsuo Oshida 6, Hideki Endo 7 & Masaharu Motokawa 8
1,5 Institute of Ecology and Biological Resources, Vietnam Academy of Sciences and Technology, 18 Hoang Quoc Viet Road Hanoi, Vietnam
2,3 Wildlife At Risk, 202/10 Nguyen Xi, Ward 26, Binh Thanh District, Ho Chi Minh City, Vietnam
4 Department of Zoology, Hungarian Natural History Museum, H1088 Budapest, Baross u.13, Hungary
6 Laboratory of Wildlife Biology, Obihiro University of Agriculture and Veterinary Medicine,
Obihiro 080-8555, Japan
7 The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
8 Kyoto University Museum, Kyoto University, Sakyo, Kyoto 606-8501, Japan
1 ntson@iebr.vast.vn (corresponding author), 2 osheatj@msn.com, 3 Jeff.Gore@MyFWC.com,
4 csorba@nhmus.hu, 5 vttu@iebr.ac.vn, 6 oshidata@obihiro.ac.jp, 7 hendo@um.u-tokyo.ac.jp,
8 motokawa.masaharu.6m@kyoto-u.ac.jp
doi: http://dx.doi.org/10.11609/jott.2785.8.7.8953-8969 | ZooBank: urn:lsid:zoobank.org:pub:CF64B7A1-5162-4101-80FF-32CCB4217BC6
Editor: Paul Bates, Harrison Institute, Kent, United Kingdom. Date of publication: 26 July 2016 (online & print)
Manuscript details: Ms # 2785 | Received 11 May 2016 | Final received 30 June 2016 | Finally accepted 07 July 2016
Citation: Son, N.T., T.J. O’Shea, J.A. Gore, C. Gabor, V.T. Tu, T. Oshida, H. Endo & M. Motokawa (2016). Bats (Mammalia: Chiroptera) of the southeastern Truong Son Mountains, Quang Ngai Province, Vietnam. Journal of Threatened Taxa 8(7): 8953–8969; http://dx.doi.org/10.11609/jott.2785.8.7.8953-8969
Copyright: © Son et al. 2016. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use of this article in any medium, reproduction and distribution by providing adequate credit to the authors and the source of publication.
Funding: Wildlife At Risk, Vietnam Academy of Science and Technology, JSPS Ronpaku Program, and SYNTHESYS Project, financed by the European Community Research Infrastructure Action under the FP7 “Capacities” Program, Hungarian Scientific Research Fund (OTKA).
Conflict of Interest: The authors declare no competing interests.
For Vietnamese abstract, Author Details and Author Contribution see end of this article.
Acknowledgements: Nguyen Vu Khoi and Wildlife At Risk sponsored and guided the field work, and the director and researchers of IEBR provided support. We thank biologists in other disciplines who participated in field work, including C. Abercrombie, R. D. Babb, L. V. Cuong, P. Moler, B. H. Manh C. Hope, W. Van Devender, T. A. Vu; E. J. Sterling (New York), K. Kevin (Berkeley), and B. H. Manh provided the study area map. Fieldwork was approved and supported by FPD of Quang Ngai Province and the Ministry of Agriculture in Hanoi. Precipitation data were obtained from the NASA Langley Research Center POWER Project. Nguyen Truong Son was supported by JSPS RONPAKU Program ID No. VAST–11125 and JSPS Core-to-Core Program B. Asia-Africa Science Platforms (2014-2016). Gabor Csorba received support from the SYNTHESYS Project, financed by the European Community Research Infrastructure Action under the FP7 “Capacities” Program and the Hungarian Scientific Research Fund (OTKA) K112440. N.V. Khoi and R. D. Babb kindly contributed photographs.
Abstract: Bat communities of mainland Southeast Asia can be highly diverse. Many are under threat. Despite this, regional faunal composition is not well documented for many areas, including regions of Vietnam. We assessed the biodiversity of bats in a watershed protection forest in the southeastern Truong Son (Annamite) Mountains, southwestern Quang Ngai Province, Vietnam in 2011–2013. Twenty species of insectivorous bats were documented including a high diversity of Murina species Tube-nosed Bats. Diversity and abundance indices were compared with that recorded previously in two nature reserves and one national park in Vietnam, and were higher or comparable in several measures despite the lack of a karst substrate for roosts. Reproduction in the insectivorous bat fauna coincided with the early rainy season. In the late dry season, pregnant females of several species were observed but volant juveniles were not present, whereas in the early wet season adult females were lactating or post-lactating and volant juveniles of nine species were detected. We recorded echolocation calls of 14 bat species; for each species, we compared features of calls with those reported previously in other Asian localities. For some species we found discrepancies in call metrics among studies, perhaps suggesting a greater hidden biodiversity of bats in Southeast Asia.
Keywords: Bats, Chiroptera, diversity, echolocation, reproduction, Vietnam.
INTRODUCTION
Bat communities in Southeast Asia are among the most diverse in the world but are threatened by habitat loss and other factors (Kingston 2010). Despite high diversity, there is little descriptive documentation available on the faunal composition of regional bat communities in mainland Southeast Asia, including a lack of basic information on echolocation patterns and the timing of reproduction of species within these bat communities. The Truong Son Mountains of Vietnam and the adjacent Lao People’s Democratic Republic (Lao PDR) have high faunal biodiversity in general (Tordoff et al. 2003), but little is known about bat diversity in this mountain range. Therefore, our study had three objectives: (1) to document the bat fauna of the southeastern Truong Son Mountains and to compare its diversity with that reported previously in other localities of Vietnam (Hendrichsen et al. 2001; Furey et al. 2010); (2) to sample characteristics of echolocation calls of a subset of the insectivorous bats of the southeastern Truong Son Mountains, and to qualitatively compare their echolocation traits with those reported previously in other localities in Asia; (3) to assess the timing of reproduction in female bats in the late dry season and in the early wet season. This region is influenced by a predictable rainy season following the dry winter season (Sterling et al. 2006; NASA 2012). Seasonal patterns in reproduction of tropical insectivorous bats wherein the birth and fledging of young occur during rainy seasons when primary productivity and insect abundance are high have been observed in other tropical regions (e.g., Fleming et al. 1972; Bernard & Cumming 1997; Racey & Entwistle 2000), including one reserve in northern Vietnam (Furey et al. 2011).
MATERIALS AND METHODS
Study area
We sampled bats in southwestern Quang Ngai Province, Vietnam. The study area is a Watershed Protection Forest administered through the Quang Ngai Forest Protection Department, Vietnam Ministry of Agriculture and Rural Development, which facilitated our study. The forest is located in central Vietnam in the southeastern Truong Son (Annamite) Mountains, Ba To District, southwestern Quang Ngai Province (Fig. 1). The study area is near the borders with Gia Lai Province, Kon Tum Province, and Binh Dinh Province.
We based our work at two campsites (Fig. 1): Camp 1 was at 750m elevation, and was sampled in late May – early June 2011 (early rainy season) and March 2013 (late dry season); Camp 2 was at 930m elevation and was sampled in March 2012 (late dry season). Camp 1 was in a cleared grassy area at coordinates 14.66020N & 108.60750E. The surrounding forest was mainly secondary regrowth after logging about 40 years earlier. Camp 2 was located at 14.62060N 108.58650E and was also covered by secondary forest but had a greater number of mature and large diameter trees compared to those of Camp 1. Both sites are in a region that experiences highly seasonal rainfall (Fig. 2).
We compare our results with previous studies on bat biodiversity conducted at three other localities in Vietnam that have higher conservation status: Kon Cha Rang Nature Reserve (14.5670N & 108.5670E) and Kon Ka Kinh National Park (14.3330N & 108.3670E) in Gia Lai Province (Hendrichsen et al. 2001) and Kim Hy Nature Reserve in Bac Kan Province in northern Vietnam (Furey et al. 2010). The studies in Gia Lai Province took place for 2-3 weeks in each reserve during March and April 1999; Kon Ka Kinh National Park and Kon Cha Rang Nature Reserve are about 42km and 10km away from our study area, respectively. Estimation of assessment effort and relative abundance are not available for the Gia Lai studies (Hendrichsen et al. 2001), limiting quantitative comparisons. However, we also compare our results with the study by Furey et al. (2010) at Kim Hy Nature Reserve, the most comprehensive study of a bat community in Vietnam. Unlike our study area, Kim Hy Nature Reserve has a karst substrate (Furey et al. 2010).
Bat sampling, identification, and reproductive assessment
We captured bats using mist nets and harp traps set from ground level. We set nets across trails in forest, over small ponds and streams in forest or near forest edges, and at openings at the forest edges. We set harp traps at similar locations and in dry stream beds that could function as travel corridors for bats. We deployed two different harp traps in 2011. One was a 4-bank trap 1.5x1.5 m in area (2.25m2) and the other was a 2-bank trap 0.9x1.1 m in area (1.0m2). In 2012 we deployed the same size traps and a larger 4-bank trap 2m x 2m in area (4m2). Mist nets ranged from 6.0 to 12.8 m in length. We sampled for bats near the lower elevation Camp 1 at 33 geo-referenced locations on 11 nights between 28 May and 9 June 2011 inclusive, and on five nights 16 to 20 March 2013 inclusive. In 2011 most (90%) sampling localities were within 800m of Camp 1 with a maximum distance of 1.25km between localities; elevations at netting sites in 2011 varied from 712m to 772m. At Camp 2 we sampled at 52 geo-referenced locations on nine nights between 12 and 20 March 2012 inclusive. Most of these sampling locations (45 of 52) ranged from 883 m to 991 m in elevation and were within 800m of Camp 2, but for two nights nets were set at 330–650 m elevation. In March 2013 we sampled for five nights using the same-sized mist nets as during prior trips and two 2.25m2 harp traps. All capture and handling procedures for bats were approved by the Institute for Ecological and Biological Resources, Vietnam Academy of Sciences.
We relied on the following sources for identifications of bats in the field based on external characters: Borissenko & Kruskop (2003), Francis (2008), and Kruskop (2013). We also compared specimens in the field with recent descriptions of new taxa that appeared in Kruskop & Eger (2008) and Furey et al. (2009b). In the laboratory we also compared voucher specimens with descriptions of new Murina species by Csorba & Bates (2005), Csorba (2011), Csorba et al. (2007, 2011), Eger & Lim (2011), Francis & Eger (2012), Soisook et al (2013a,b), and Son et al. (2015a, b). We preserved voucher specimens in 95% ethanol. We also took liver or wing tissue in 95% ethanol for future DNA analysis (Son et al. 2015a). All samples and voucher specimens are in collections at the Institute for Ecological and Biological Resources, (IEBR) at the Vietnam Academy of Sciences and Technology, Hanoi.
We categorized adult female bats as pregnant, lactating, post-lactating, and non-reproductive according to criteria of Racey (2009). We recorded number of visible embryos per female when pregnancy was detected in voucher specimens. Age was categorized as volant juvenile or adult based on fusion of the phalangeal epiphyses (Brunet-Rossinni & Wilkinson 2009).
Echolocation recordings
We recorded echolocation sounds of bats in 2011 and 2012, including individuals prepared as voucher specimens. We compared our results with those reported in the literature for the same species recorded elsewhere in Asia. Such comparisons can be useful for future species identification, particularly for cryptic taxa that may be members of species complexes that are not yet well understood (Francis 2008). We recorded calls in three situations: (1) single bats flying in an enclosure made with mosquito nets (2m high x 2m wide x 3m long); (2) single bats hanging freely on the sides of the enclosure; (3) single bats held in our hands. Recordings of bats in flight in enclosures or in hand are commonly employed in bat studies in Asia (e.g., Kingston et al. 1999; Kingsada et al. 2011; Hughes et al. 2011) but some measurements can be biased compared to recordings of free-flying bats. However, given the low capture success (see Results) and need for voucher specimens we chose not to release bats for recordings in the open.
In 2012 we sampled echolocation calls as WAV files using an Echometer EM 3 digital ultrasonic recorder (Wildlife Acoustics 2012). The EM3 allows recording at sampling rates of 256 and 384 kHz (providing analysis of calls up to frequencies of about 192 kHz). We set the recording amplitude threshold at 18 db. We analyzed properties of calls recorded in 2012 in Hanning windows using spectrograms, oscilloscope tracings, and power spectra features of Call Viewer software set at 10 db background threshold and 256-point FFTs (Skowronski & Fenton 2008). We analyzed time and frequency characteristics for 12 representative calls per individual. For bats with predominantly constant frequency (CF) calls we calculated the frequency of maximum energy (FMAXE, kHz), the frequency range of the preceding upsweep (FM rise, kHz), the frequency range of the terminal downsweep (FM tail, kHz), and the sound duration (ms). For bats with predominantly frequency modulated (FM) calls we calculated mean ± SD and ranges for start frequency (kHz), end frequency (kHz), FMAXE (kHz), midpoint (kHz) and duration (ms). We did not measure interpulse intervals because of the confined recording context. In 2011 recordings were made with AnaBat II bat detectors with programmable zero-crossing analysis interface modules (AnaBat™ CF Storage ZCAIM; Titley Electronics, NSW, Australia). We used AnalookW software, version 3.8.13 (http://users.lmi.net/corben/WinAnalook.htm) to view and describe the calls recorded in 2011. This system allows time and frequency measurements of fundamental harmonics, but does not allow more thorough acoustic analysis (Fenton et al. 2001). The Anabat system also does not allow reliable measurements of the upper ranges of echolocation calls of species that utilize very high frequencies. In our study areas these were primarily bats of the genera Murina and Kerivoula. Murina species produce calls that are faint in intensity, making upper frequencies difficult to record. We provide results from Anabat recordings for those species of Murina that were recorded only in 2011 with the caveat that start frequencies are likely underestimates. For comparative purposes we also tabulate these same metrics from the echolocation calls of the same species reported previously elsewhere in Asia.
Computations and statistical analyses
We provide original data and simple descriptive summary statistics: means, standard deviations (SD), ranges, and coefficients of variation (CV; SD/mean). We calculated metrics for insectivorous bat species diversity for comparison with the insectivorous bat communities described in the three other bat diversity assessments in Vietnam noted above following methods given by Kingston (2009) and Furey et al. (2010). We calculated assessment effort based on total surface areas of mist nets and harp traps multiplied by the number of hours nets or traps were set, and estimated the success rates by dividing total number of individuals or total number of species captured per unit effort. We provide species richness (S) as the total number of species in a community. We calculated species diversity indices, measures of evenness of distribution of individuals among species, predicted species richness, and inventory completeness using program SPADE (Chao & Shen 2010). We calculated the inverse Simpson Index of Diversity as 1/D where D = [Σn (n –1)]/ [N (N–1)], where n is the number of individuals in each observed species, and N is the total number of individuals captured (Magurran 1988). Evenness of the distribution of individuals among species is expressed by the formula (1/D)/S, where S is the number of observed species. We followed Furey et al. (2010) and used program SPADE to calculate predicted species richness based on a hypothetical increase in sampling effort that was double the number of bats captured; we estimated predicted species richness with two methods (Solow & Polasky 1999; Shen et al. 2003), and then measured inventory completeness as the range in the ratio of observed species richness to predicted species richness x 100% based on the two estimation computations.
RESULTS
Species diversity
We detected 20 species of bats among the 166 individuals captured at the study area (Table 1). We collected 98 entire specimens with corresponding tissue samples (muscle or liver). We also took wing tissue from another 15 specimens. Seven species were captured only in mist nets, five only in harp traps, and eight in both (including four of the five species of Murina; Table 1). Abundance of bats and number of species detected per unit of mist netting effort were about a tenth of those detected per unit of harp trapping effort (Table 1).
At the Camp 1 area we captured 97 bats of 17 species (Table 1) at 15 sampling locations in 4,177 m2nh of mist net and 390 m2th of harp trap sampling (both years combined, Table 1). The number of species detected and individuals detected per unit effort was lower at the higher elevation sites sampled at Camp 2 in 2012, where Rhinolophus affinis was preponderant (Table 1). We captured 69 bats in 2012, and 65 of these were captured within the 883–991 m elevation range. The respective numbers of individuals and species detected per effort unit were lower at Camp 2 localities than at Camp 1 localities (Table 1).
Individuals of the five species of Murina captured at Camp 1 in 2011 were taken at locations within 630m horizontal distance of each other, with three species of Murina taken at the same trap or net site. Although no fruit bats (Pteropodidae) were captured or seen in the study area, on 21 March 2012 we observed bat-expressed fruit pulp on the ground beneath a fruiting tree at 825m elevation and in June 2011 Cynopterus bats were observed near the village of Ba To, elevation 53m, about 17km from our study area.
Simpson’s Inverse Index of Diversity and Index of Evenness were higher at the lower elevation areas near Camp 1 sampled in 2011 and 2013 in comparison with areas near Camp 2 sampled in 2012 (Table 2). Inventory completeness at the Quang Ngai study area was estimated to be 85–87 %, with a predicted 23–24 species likely to be detected with a doubling in numbers of bats captured (Table 2). More species were predicted at the Camp 1 lower elevation sites than at the Camp 2 higher elevation sites, with similar inventory completeness estimates (72%) for both (Table 2).
Seasonality in female reproduction
In late May and June 2011 (early in the rainy season), we captured volant juveniles of nine species and adult females of six species; most of the adult females were lactating or post-lactating (19 of 23) with three pregnant and one non-reproductive (Table 3). In March 2012 and 2013 (prior to the rainy season), no female bats were lactating or post-lactating, no volant juveniles of either sex were captured, and most female bats taken were either pregnant (36 of 56) or had no discernible evidence of pregnancy or lactation (Table 3). A single embryo was found in each of the pregnant females saved as voucher specimens; the following species and number of pregnant individuals (in parentheses) were examined for number of embryos by dissection: Hipposideros cineraceus (1), H. larvatus (1), Kerivoula hardwickii (1), My. muricola (1), R. affinis (4), and R. pusillus (6).
Echolocation calls
We recorded echolocation calls of 14 species of bats in the southeastern Truong Son Mountains (Tables 4 and 5). To our knowledge, calls of four species (M. annamitica, M. beelzebub, M. eleryi, and M. fionae) have not been previously reported. FM calls of four species (K. hardwickii, M. cyclotis, Myotis ater, and My. muricola) were generally concordant with those reported previously (Table 4). Differences with calls reported in the literature for some but not all localities were found for Scotomanes ornatus and four species with CF calls: R. affinis, R. pearsonii, R. pusillus, and H. larvatus (Table 5; see Discussion).
DISCUSSION
Comparisons with three protected areas in Vietnam (Furey et al. 2010; Hendrichsen et al. 2001) suggest that the bat fauna of the southeastern Truong Son Mountains in Quang Ngai Province is diverse for a region that does not have a karst geological substrate (karst provides many potential roosting sites). Greater species richness of insectivorous bats was found at our study area than in Kon Cha Rang Nature Reserve and Kon Ka Kinh National Park (15 and 13 species, respectively; Hendrichsen et al. 2001) in nearby Gia Lai Province, but overall diversity was lower than at the more intensively sampled, karst-dominated Kim Hy Nature Reserve (28 species of insectivorous bats, four pteropids, 90% inventory completeness, Simpson Index 10.91 ± 0.18, Evenness 0.341; Furey et al. 2010). Abundance of bats per unit of mist-netting effort was twice as high at Kim Hy Nature Reserve (0.014 bats per m2nh, Furey et al. 2010) than at our area, but results per unit trapping were similar (0.047 bats per m2th; Furey et al. 2010). Species detected per unit of mist-netting was nearly identical (0.0009; Furey et al. 2010), but species detected per unit trapping (0.006 at Kim Hy; Furey et al. 2010) was higher at our study area overall. The number of species and individuals detected per unit effort at the lower elevation site we sampled in 2011 and 2013 were comparable to or higher than at Kim Hy overall, and comparable to or higher than two of the three forest types at Kim Hy Nature Reserve (Furey et al. 2010). Lower evenness and diversity was especially pronounced at our higher elevation sites sampled during 2012; diversity comparisons are more similar among our lower elevation sites sampled during 2011/2013 and the sites at Kim Hy Nature Reserve.
It is noteworthy that we documented five species of tube-nosed bats (genus Murina) sympatrically distributed at the study area. Son et al. (2015a) provided a detailed overview of the genus Murina in Vietnam, and established that Vietnam has the greatest number of species of Murina in Southeast Asia. In contrast, however, we did not detect fruit bats at our study area. At least two species of fruit bats were captured at Kon Cha Rang and Kon Ka Kinh National Park in nearby Gia Lai Province (Hendrichsen 2001), and four species of fruit bats were present at Kim Hy Nature Reserve in Bac Kan Province (Furey et al. 2010). Pteropodid bats may utilize the southeastern Truong Son Mountains study area at other times of the year if fruit is more abundant than in the dry or in the early wet seasons when we sampled the bat fauna. Evidence for the presence of fruit bats of unknown species was detected below a fruiting tree near the 2012 study area, and in 2011 an unidentified Cynopterus was seen about 17km from our camp at a lower elevation.
We found a higher diversity of bats at the lower elevation site. Only M. eleryi was taken exclusively in a harp trap at this site, suggesting that differences in sampling techniques cannot explain the higher diversity at the lower elevation. Two ecological factors may contribute to the differences in diversity between lower and higher elevations in the southeastern Truong Son Mountains. In other tropical and subtropical areas, the diversity of bats declines with increasing elevation (e.g., Graham 1983; Patterson et al. 1998). Additionally, some differences in diversity between lower and higher elevations at our study area might reflect seasonal movements of bats. In northern Vietnam Furey et al. (2010) suggest that some species of bats may be unique to each season. They found only about half of the total documented species in both dry and wet seasons (40–52 % depending on habitat type), and fewer species were recorded in each unique habitat type during the wet season than during the dry season (Furey et al. 2010).
We found evidence for seasonal differences in reproduction of female bats at our study area. In much of Vietnam there is a predictable rainy season following a dry winter season, but with the monthly patterns of precipitation varying regionally (Sterling et al. 2006). In many other tropical and subtropical parts of the world the reproductive season of insectivorous bats is timed to coincide with predictable rainy seasons: young are born and become independent when community productivity and insect abundance is high (Fleming et al. 1972; Bernard & Cumming 1997; Racey & Entwistle 2000). Furey et al. (2011) found strong evidence to support the existence of this pattern in the insectivorous bat fauna at Kim Hy Nature Reserve, and suggested that the pattern may hold for a wider region in Southeast Asia. Rainfall in the southeastern Truong Son Mountains is lowest in January through March, then increases and remains relatively higher from May to November (Fig. 2). Our findings strongly support Furey et al.’s (2011) suggestion of rainy season reproduction of bats in Vietnam. In March prior to the rainy season, we found that many females were pregnant, no females were lactating or post-lactating, and no volant juveniles of either sex were captured (Table 3). In late May and June, most adult females were lactating, a few were pregnant, and volant juveniles of 10 species were captured (Table 3). Given the longer period of seasonal rainfall at our study area compared to the Kim Hy Nature Reserve, it is possible that the reproductive season for some species of bats also may be more prolonged than in areas with shorter rainy seasons.
Echolocation call measurements of the two Murina species recorded in 2012 (Table 4) are concordant with those reported previously for other species in this genus. Kingston et al (1999) and Thong et al. (2011) reported that echolocation calls of different Murina species tend to be similar to one another, showing short durations and faint intensity, sweeping a broad bandwidth with high frequency starting points, typically at about 150kHz. These characteristics match those we recorded for M. beelzebub and M. fionae. Calls for the Murina sampled at Camp 1 in 2011 also match these characteristics, but our start frequency estimates may have been limited by the equipment used at that time. For these species, the maximum values in the range of the start frequencies are most reliable. Midpoint values may also be biased low. However, our measurements of calls of M. cyclotis in 2011 are very similar to those of M. cyclotis from Thailand (Hughes et al. 2011; Table 4). Our measurements of echolocation calls of the other species of vespertilionid bats are consistent with those reported previously. Echolocation calls of Scotomanes ornatus were recorded from a hand-held individual in our study, and the start and end frequencies are higher than those reported by Furey et al. (2009a) for free-flying S. ornatus. This is most likely because the free-flying individuals emphasized the first harmonic, whereas our peak energy measurements of the hand-held bat were all in the second harmonic. Measurements of calls of S. ornatus recorded by Liu et al. (2011) at Mianyang, China had lower start frequencies than our results, but showed similar FMAXE and end frequencies (Table 4).
Greater discrepancies in echolocation call measurements are observed when we compare CF calls of rhinolophid and hipposiderid bats recorded in the southeastern Truong Son Mountains with those previously reported in other parts of Asia (Table 5). It is suspected that several currently recognized species of these Asian bats, such as H. larvatus and some species of Rhinolophus, may consist of complexes of several species with very similar morphological characteristics (Francis 2008). Further research will be required to resolve the causes of geographic variation in echolocation calls of rhinolophid and hipposiderid bats in relation to their systematic status. Such geographic variation is found in FMAXE measurements of R. affinis (Table 5). In R. affinis, the coefficient of variation was <1% for FMAXE of 216 calls from 18 bats recorded at our study area in Quang Ngai, whereas calls recorded previously in Vietnam, China, Lao PDR, Myanmar, Malaysia, Borneo and Sumatra (but not central Java) were generally outside of the range of minimum-maximum values from our study area (Table 5; Ith et al. 2015). In our study area the higher FMAXE of echolocation calls of R. affinis (sensu lato) did not follow the geographic trend suggested by Ith et al. (2016) of lower frequencies north of the Kangar-Pattani Line across the Thai-Malay Peninsula. Discrepancies also are found between calls of R. pusillus in the present study and those from some locations in China, Thailand, Lao PDR, and Vietnam (Table 5). Jiang et al. (2010) show that resting frequencies in R. pusillus across southeastern China vary by sex, location and mean annual rainfall. However, the mean frequencies in that study are outside the range of call measurements taken at our study area (Table 5). Considering this variability in echolocation calls, our findings support Zhang et al. (2009) and Soisook et al.’s (2016) suggestions that cryptic species of an R. pusillus complex might be present in Asia based on differences in echolocation calls. Values of FMAXE for R. pearsonii also showed some discrepancies as well as similarities among localities. Among hipposiderids, we found overlap with our range of estimates of FMAXE for H. pomona and published reports from elsewhere, including China, Lao PDR, Myanmar and Thailand (Table 5). In contrast, great variation is seen in FMAXE of bats referred to as H. larvatus across Asia, with results reported from Myanmar more consistent with those of bats we recorded than from many other locations (Table 5). Thabah et al. (2006) suggested that bats from Myanmar with echolocation frequencies similar to the bats we sampled may be a species other than H. larvatus. Hipposideros larvatus seems to present another case where additional research on variability in echolocation and systematics is needed. There is a possibility that some of the discrepancies that we highlight among various published studies by others could be an artifact of misidentification of bats, circumstances of recording (e.g., in free-flying vs. in-hand), or variability in equipment among studies. Nonetheless the number of differences suggests a real biological basis for this variation and the need for further study.
CONCLUSION
This study revealed significant biodiversity in the insectivorous bats of the southeastern Truong Son Mountains in Quang Ngai Province, Vietnam. Enhanced conservation and protection planning for the watershed protection forests within this area will be critical for maintaining the diversity of bats and other wildlife of the region in the future.
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Vietnamese abstract: Việt Nam được đánh giá là một trong những trung tâm đa dạng dơi trong khu vực Đông Nam Á cũng như của thế giới. Các nghiên cứu gần đây cho thấy, Việt Nam còn chứa đựng tiềm năng đa dạng các loài dơi cần tiếp tục được nghiên cứu. Từ 2011 đến 2013, chúng tôi đã điều tra đánh giá mức độ đa dạng các loài dơi tại khu rừng phòng hộ khu vực đông nam dãy Trường Sơn, trên địa bàn tỉnh Quảng Ngãi và đã ghi nhận được 20 loài dơi ăn côn trùng với mức độ đa dạng cao của các loài dơi mũi ống giống Murina. So sánh với một số khu vực khác của Việt Nam, các chỉ số đa dạng và phong phú các loài dơi ghi nhận tại vùng nghiên cứu tương đương hoặc cao hơn, mặc dù tại đây không phải là khu vực núi đá vôi, nơi trú ngụ thích hợp cho các loài dơi. Mùa sinh sản của các loài dơi muỗi được ghi nhận diễn ra vào đầu mùa mưa khi ghi nhận được đa phần các cá thể cái đang nuôi con hoặc đang cai sữa và con non có thể bay được. Trong khi cuối mùa mưa, không bắt gặp con non mà chỉ ghi nhận được số ít cá thể cái vẫn đang mang thai. Tín hiệu siêu âm của 14 loài dơi đã được ghi nhận và so sánh với những dẫn liệu công bố trước đây tại khu vực khác nhau ở châu Á mà một số điểm bất thường trong các chỉ số tín hiệu siêu âm của một số loài có thể chỉ ra rằng, sự đa dạng dơi tại Đông Nam Á còn ẩn chứa nhiều điều cần tiếp tục được nghiên cứu.
Author Details: Nguyen Truong Son and Vuong Tan Tu are interested in the taxonomy, phylogeny and status of bats, rodents and shrews. They intensively focus on bat research and conservation in Vietnam and throughout Southeast Asia. Thomas J. O’Shea has conducted studies on bats, sirenians, and other groups of mammals in the western United States and Florida, as well as in Africa, Asia, Oceania, South and Central America. He is semi-retired and has been working on biodiversity surveys with Wildlife at Risk since 2011. Jeff Gore is a wildlife biologist whose primary interest is the ecology and conservation of mammals, particularly bats. He works for a government agency in the United States and since 2009 he has helped Wildlife at Risk conduct studies of the biodiversity of bats in Vietnam. Gabor Csorba is the Deputy General Director of the Hungarian Natural History Museum. He has been working on Southeast Asian bats for 25 years; his main interest is their taxonomy, systematics, zoogeography and conservation biology. Hideki Endo, Tatsuo Oshida, and Masaharu Motokawa are professional researchers in Japan and also in Southeast Asia, focusing on the anatomy, phylogeny, and taxonomy of small mammals and other animals in Japan and Southeast Asia. They also are experts in International Education.
Author Contribution: Thomas J. O’Shea and Nguyen Truong Son worked with the team in fieldwork, data analysis, species indentification, writing, and correcting the proof: Gabor Csorba and Vuong Tan Tu: species identification; Jeffery A.Gore participated in field sampling, data collection, and reviewing manuscript; Hidedi Endo, Tatsuo Oshida, Masaharu Motokawa: reviewing manuscript.