Mammalia 2021; 85(2): 189–192
Short note
Huan-Wang Xie, Xingwen Peng, Chunlan Zhang, Jie Liang, Xiangyang He, Jian Wang, Junhua Wang, Yuzhi Zhang and Libiao Zhang* First records of Hypsugo cadornae (Chiroptera: Vespertilionidae) in China https://doi.org/10.1515/mammalia-2020-0029 Harrison 1987). In 2005, Bates et al. described Hypsugo Received March 25, 2020; accepted August 4, 2020; published online pulveratus as a species morphologically similar to H. cador- August 27, 2020 nae (Bates et al. 2005). Whereas H. pulveratus is widely distributed in China (IUCNredlist, Wilson and Reeder 2005), Abstract: Hypsugo cadornae bats have been found in In- H. cadornae was not found there yet. dia, Myanmar, Thailand, Vietnam, Laos, and Cambodia. In H. cadornae was first discovered in north-eastern India 2017 and 2018, 15 medium size Hypsugo bats were collected (Thomas 1916) and later found in India, Myanmar (Bates from Shaoguan, Guangzhou, and Huizhou in Guangdong, and Harrison 1997), Thailand (Hill and Thonglongya 1972), China. Molecular and morphological examinations iden- Vietnam (Kruskop and Shchinov 2010), Laos (Görföl et al. tified them as H. cadornae. This is the first record of 2014), and Cambodia (Furey et al. 2012). In 2017 and 2018, H. cadornae in China. Morphological and ultrasonic char- we captured 15 medium size Hypsugo bats from Shaoguan, acteristics of H. cadornae were compared with its close Guangzhou, and Huizhou in Guangdong, China. Three relative, Hypsugo pulveratus. individuals from the three different cities were carefully Keywords: echolocation calls; Hypsugo; morphology; examined. phylogeny. Nine body and 12 skull morphological features were measured using a vernier caliper (0.01 mm) according to Hypsugo cadornae was formerly classified as a subspecies of Bates and Harrison (1997); Furey et al. (2012). Compared Hypsugo savii (Ellerman and Morrison-Scott 1951) or Hyp- with H. pulveratus, H. cadornae (Figure 1A) bats have a sugo lophurus (Corbet and Hill 1992). Because of strikingly less distinctive dorsal pelage (Bates et al. 2005; Görföl differences in skull and baculum, it was later separated from et al. 2014). The forearm length ranged from 31.7 to fi H. savii and H. lophurus and considered as a distinct species 37.1 mm. The fth metacarpal was nearly as long as the (Bates et al. 1997, 2019; Corbet and Hill 1992; Hill and third and fourth metacarpal (Table 1). On the skull, the rostrum was short and narrow; the nasal notch was broad and round (Figure 1B–E, Table 1). The braincase Huan-Wang Xie, Xingwen Peng and Chunlan Zhang: These authors was full and rounded with a shallow sagittal crest in the contributed equally to this study. midpart. The cranial profile lacked a frontal depression between the rostrum and braincase. The palate was *Corresponding author: Libiao Zhang, Guangdong Key Laboratory of short, but zygomata were relatively robust with post- Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong orbital eminences. The first upper premolar (P2) was Institute of Applied Biological Resources, Guangdong Academy of very short and was smaller than that of H. pulveratus. Sciences, Guangzhou, 510070, China, E-mail: [email protected] Genomic DNA was isolated from the muscle cells of Huan-Wang Xie, Xingwen Peng and Chunlan Zhang, Guangdong Key each of the three bats. Polymerase chain reaction was Laboratory of Animal Conservation and Resource Utilization, then performed to amplify a portion of the mitochondrial Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological Resources, cytochrome b gene (CYTB; 1140 bp) using primers CY1 Guangdong Academy of Sciences, Guangzhou, 510070, China (5′-TAG AAT ATC AGC TTT GGG TG-3′) and CY2 (5′-AAA Jie Liang, Xiangyang He, Junhua Wang and Yuzhi Zhang, Guangdong TCA CCG TTG TAC TTC AAC-3′) (Li et al. 2006) and a Key Laboratory of Animal Conservation and Resource Utilization, fragment of the cytochrome oxidase c subunit I gene Guangdong Public Laboratory of Wild Animal Conservation and (COI;657bp)usingprimersBat5310(5′-CCT ACT CRG CCA Utilization, Guangdong Institute of Applied Biological Resources, TTT TAC CTA TG-3′) and R6036 (5′-ACT TCT GGG TGT CCA Guangdong Academy of Sciences, Guangzhou, 510070, China ′ Jian Wang, School of Life Sciences, Sun Yat-sen University, AAG AAT CA-3 ) (Robins et al. 2007). The PCR products Guangzhou, 510275, China were sequenced (GenBank accession numbers of the
Open Access. © 2020 Huan-Wang Xie et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 International License. 190 H-W. Xie et al.: Hypsugo cadornae in China
Figure 1: (A) Portrait of a living Hypsugo cadornae (B) Dorsal, (C) lateral, and (D) ventral views of the skull and occlusal and lateral views of the mandible of an H. cadornae bat (GD-181117 from Huizhou City, China). newly generated sequences; CYTB ds625, MN508627, Adaptation to environments is a possible reason for MN508628; COI MN508629, MN508631, MN508632). The the distribution of H. cadornae bats throughout the alignment of sequences was performed using concate- Indomalayan region. It has been reported that H. cador- nated CYTB and COI sequences of known H. cadornae nae can roost on banana trees or a dry bamboos in a fi and other ve related bat species (Figure 2) with MEGA X lowland forest (Bates et al. 2005). In our surveys, (Kumar et al. 2018). The Maximum-likelihood phyloge- H. cadornae bats were captured from an old building, a netic tree was constructed based on the Hasegawa- concrete bridge, and sabal trees in villages, which were Kishino-Yano model. Bootstrap support with 1000 rep- partly or entirely surrounded by lowland forests. More licates was analyzed with the percentage cut-off of 50%. All three examined individuals (GD-172497, GD-180937, surveys with a wider scope are warranted to discover and GD-181117) were found to be phylogenetically clus- new species of bats and to understand their ecological tered with H. cadornae bats with 100% bootstrap value conditions. Presented first records of H. cadornae in but were separated from other species of Hypsugo bats China enlarged the range of the species distribution in (Figure 2). Therefore, based on morphological features south-eastern Asia (IUCNredlist, Lim et al. 2016). This and molecular data, examined individuals were identi- study advanced our knowledge of bat distribution and fied as H. cadornae. provided important information for further studies of Echolocation calls of the three H.cardonae bats various aspects of H. cadornae in China. were recorded using an Avisoft Bioacoustics USG 116(e) detector equipped with an Avisoft FG microphone. The spectrograms were generated by 512 consecutive fast Acknowledgments: We thank Haitao Huang for helping Fourier transforms (FFT) at 96.87% frequency over- with the photography. We also thank Yi-Hsuan Pan and lapped with a Hamming window using the Avisoft- Prof. Chao-Hung Lee for valuable advice. SASLab Pro software. Echolocation calls of H. cadornae Author contributions: Libiao Zhang, Huan-Wang Xie, were found to be in frequency-modulation (FM), usually Xingwen Peng, Xiangyang He, Jian Wang, Junhua Wang, with multiple harmonics. Thirty relatively clear sound and Yuzhi Zhang collected the bats. Jie Liang and Chunlan waves of each bat were randomly selected for analysis. Zhang performed the experiments. Huan-Wang Xie, The maximum energy of calls was mostly in the first Xingwen Peng, Chunlan Zhang, Jie Liang, and Libaio harmonic. The peak frequency with the maximum en- Zhang analyzed the data. Libiao Zhang, Huan-Wang Xie, ergy was 38.81 ± 1.34 kHz. This is a relatively low fre- Xingwen Peng, and Jie Liang wrote the manuscript. quency suitable for hunting insects with thick Research funding: This work was supported by funds exoskeletons such as beetles, bugs, and butterflies allocated for Background Survey of Terrestrial Wildlife (Weterings et al. 2015). The highest frequency was in Guangzhou (SYZFCG-[2017]032), Diversity Survey of found at 65.60 ± 4.89 kHz, and the pulse duration was Terrestrial Vertebrate in Danxiashan National Nature 3.10 ± 0.77 ms. Reserve, GDAS Special Project of Science and Table : Selected morphological and craniodental measurements (in mm) of Hypsugo bats.
Hypsugo cadornae Hypsugo pulveratus
China Vietnam India and Myanmar Cambodia Myanmar Laos and Vietnam China
Character This study Bates et al. Bates and Harrison Furey et al. Bates et al. Görföl et al. James et al.
HB . ± .(.–.)() . M/. F .(–.)() .. ± .(.–.)() FA ± .(.–.)() M/. F .(.–.)() .. ± .(.–.)() . ± .(.–.)() . T . ± .(.–)() . M/. F .(–)() . ± .(.–.)() E . ± .(.–.)() . M/. F .(–)() .. ± .(.–.)() HF . ± .(.–.)() M/. F .(.–)() .. ± .(.–.)() . ± .(.–.)() TIB . ± .(.–.)() M/. F . ± .(.–.)() . ± .(.–.)() MET . ± .(.–.)() . M/. F .(.–.)() . ± .(.–.)() MET . ± .(.–.)() . M/. F .(.–.)() . ± .(.–.)() MET . ± .(.–.)() . M/. F .(.–)() . ± .(.–.)() GTL . ± .(.–.)() . M/. F .(.–)() .. ± .(.–.)() . ± .(.–.)() . CCL . ± .(.–.)() . M/. F .(.–.)() . . ± .(.–.)() . ± .(.–.)() . ZB . ± .(.–.)() . M/. F . . ± .(.–.)() . ± .(.–.)() .
BB . ± .(.–.)() . M/. F .(.–.)() . ± .(.–.)() . ± .(.–.)() al.: et Xie H-W. PC . ± .(.–.)() . M/. F .(.–.)() . ± .(.–.)() . C–M . ± .(.–.)() . M/. F .(.–.)() . . ± .(.–.)() . ± .(.–.)() . C–M . ± .(.–.)() . M/. F (.–.)() . . ± .(.–.)() . ± .(.–.)() M–M . ± .(.–.)() . M/. F .(.–)() .. ± .(.–.)() . ± .(.–.)() M . ± .(.–.)() . M/. F .(.–.)() . . ± .(.–.)() . ± .(.–.)() cadornae Hypsugo RW . ± .(.–.)() . M/. F .(.–.)() . ± .(.–.)() C–C . ± .(.–)() . M/. F . . ± .(.–.)() . ± .(.–.)() MAW . ± .(.–.)() . . ± .(.–.)()
Values are given in mean ± SD, min-max (n). nChina in 191 192 H-W. Xie et al.: Hypsugo cadornae in China
GD-172497/MN508628+MN508632
98 GD-180937/MN508627+MN508631
100 GD-181117/MN508625+MN508629
100 Hypsugo cadornae/MH753139+HM540624
Hypsugo macrotis/KX429685+KX429684
Hypsugo savii/AJ504450+FR856654
69 Hypsugo dolichodon/KX429687+HM540643 48 Figure 2: Maximum likelihood phylogenetic Hypsugo pulveratus/KX429686+HM540657 tree based on concatenated nucleotide sequences of fragment of CYTB and COI Pipistrellus javanicus/KX496357+KX496358 genes of different Hypsugo species. Pipistrellus javanicus was used as an 0.05 outgroup taxon.
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