Updating the occurrence of Harpiocephalus harpia (Chiroptera: Vespertilionidae) and its karyology in Taiwan / Mise à jour l'occurrence de Harpiocephalus harpia (Chiroptera: Vespertilionidae)

Mammalia (2006): 170–172 � 2006 by Walter de Gruyter • Berlin • New York. DOI 10.1515/MAMM.2006.024

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2007/13

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Updating the occurrence of Harpiocephalus harpia(Chiroptera: Vespertilionidae) and its karyology in Taiwan

Mise a jour l’occurrence de Harpiocephalus harpia (Chiroptera:Vespertilionidae) et sa karyologie a Taiwan

Liang-Kong Lin1,*, Masashi Harada2, MasaharuMotokawa3 and Ling-Ling Lee4

1 Department of Life Sciences, Tunghai University,Taichung 407, Taiwan, ROC,e-mail: [email protected] Laboratory Animal Center, Osaka City UniversityGraduate School of Medicine, Osaka 545-8585, Japan3 The Kyoto University Museum, Kyoto 606-8501,Japan4 Department of Life Science, Taiwan University,Taipei 106, Taiwan, ROC

*Corresponding author

Keywords: Harpiocephalus; karyotype; Taiwan.

The hairy-winged bat (genus Harpiocephalus) is one ofthe least-known bats of the Vespertilionidae. Harpioce-phalus ranges from India to Indochina, Taiwan and thePhilippines, and south to Indonesia and the Moluccas(Nowak 1999). However, the number of specimens fromany given locality has been limited since the discovery ofHarpiocephalus in Java in 1839 (Das 1986). Recent cap-tures are from India (Das 1986; Mandal et al. 1998),southern China (Zhang 1997), Borneo (Hill and Francis1984), Malaysia (Francis 1995), Thailand (Lekagul andMcNeely 1977; McBee et al. 1986), and Philippines (Ingleand Heaney 1992; Heaney et al. 1999). It is unclearwhether this is because it is rare or it is naturally secretive(Bates and Harrison 1997).

Harpiocephalus was considered to be monospecificand H. harpia to be monotypic (Ellerman and Morrison-Scott 1951; Koopman 1993). However, specimens foundin Burma, Thailand and Borneo were sometimes treatedas another distinct species, H. mordax (Thomas 1923;Hill and Francis 1984; Corbet and Hill 1992). Accordingto Corbet and Hill (1992), H. mordax has an expandedzygomatic width (14.4–14.5 mm in mordax, 12.1–13.9 mm in harpia) and rostral width (6.9–7.5 mm in mor-dax, 5.8–6.8 mm in harpia), with differences betweenmordax and harpia greater than the degree of sexualdimorphism.

The aim of this note is to provide an update on theoccurrence of Harpiocephalus in Taiwan and commentson its taxonomic status in terms of morphology and cra-nial characteristics. In addition, the karyotype of H. mor-dax from Thailand was identified as 2ns40, FNs62 by

McBee et al. (1986). However, because of poor fieldpreparation, the chromosome analysis was not clear asdescribed by McBee et al. (1986). This study is the firstreport on conventional, G-banded and C-banded karyo-types of Harpiocephalus from Taiwan.

The first record of this tropical species in Taiwan wasreported by Kuroda (1936), who described a specimenpurchased in Puli, Nantou County, central Taiwan. Kuro-da (1936) described the forearm length of the bat assmaller than a specimen from India. He concluded thatmore specimens were needed to clarify whether the dif-ference was due to individual variations or was an insularform. The specimen was thought to have been destroyedby fire during the Second World War (Kuroda 1952; Jones1975). Later, no additional specimens were obtained,even though the Naval Medical Research Unit No. 2,Bureau of Medicine and Surgery, Navy Department, USconducted an extensive mammal inventory of the islandduring 1960–1970 (Kuntz and Dien 1970; Lin et al. 1997).

During the years 1996–2003, we conducted a batinventory in Taiwan. Three specimens of Harpiocephaluswere captured in mountain areas. In addition, Kuroda’s1936 specimen was rediscovered in the National ScienceMuseum of Tokyo (NSMT M21174). Our first trappedspecimen was obtained on 13 April 1996, at an altitudeof 2100 m on the No. 210 logging road, Maoli County,western Taiwan. It was a scrotal male with testes meas-uring 10.0 mm=1.7 mm, and it is deposited in the TaiwanEndemic Species Research Institute, Chichi, Taiwan(TESRI M0074). The second specimen, a pregnantfemale with two embryos, was caught on 5 May 1998,at an altitude of 1120 m on the Yen-pei logging road,Taitung County, eastern Taiwan. It is deposited inthe Zoology Department, Taiwan University, Taipei(1998050501). The third female specimen was caught on16 July 2003, at an altitude of 500 m on the Nan-ann,Hualian County, eastern Taiwan. It is deposited in the LifeSciences Department, Tunghai University, Taichung(B030029). The latter individual was identified as a juve-nile, with an epiphyseal gap at the fourth metacarpal-phalangeal joint. Based on this intensive bat survey in1996–2003, we suggest that this species is rare inTaiwan.

For this study, we also examined nine specimensdeposited in the Natural History Museum, London. Thefollowing external measurements were taken: bodyweight (BW), forearm length (FA), head and body length(HB), ear length (E), tail length (T), length of tibia (TIB),and length of thumb (thumb). External measurements of

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L.-K. Lin et al.: Updated occurrence of Harpiocephalus in Taıwan 171


Figure 1 Dorsal, ventral, and left lateral views of the cranium,and left lateral view of the mandible (from top to bottom) offemale (left) and male (right) specimens of Harpiocephalus harpiafrom Taiwan. The scale bar represents 10 mm.

Table 1 Forearm length and 15 cranial measurements for Harpiocephalus harpia from Taiwan, Java, Moluccas, Bhutan, and India.

Parameter Taiwan Java Moluccas Bhutan India

Female (ns2*) Male (ns2) Female (ns3) Male (ns3) Unknown Male Female

FA, mm 49.40, 47.40 47.96, 47.50 46.59, 48.75 (ns2) 45.47, 47.38 (ns2) – – –GL, mm 20.27, 20.12 19.92, – 22.31 (22.22–22.43) 20.66, 20.8 (ns2) – – –CBL, mm 20.17, 19.39 19.04, – 20.39 (19.94–20.72) 19.00 (18.69–19.37) – – –ZW, mm 14.47, 13.46 13.13, 12.96 13.57 (13.57–13.58) 12.39 (12.36–12.45) 13.46 – 13.84IOW, mm 5.83, 5.73 5.58, 5.53 5.73 (5.70–5.76) 5.67 (5.49–5.99) 5.63 – 5.39MW, mm 11.71, 10.82 10.95, – 11.13 (10.96–11.46) 10.17, 10.41 (ns2) – – –PL, mm 9.66, 8.31 8.87, 8.76 9.63 (9.42–9.77) 8.90 (8.36–9.84) 9.06 – 9.53WM, mm 7.58, 7.32 7.27, 7.01 7.58 (7.48–7.69) 7.00 (6.92–7.09) 7.81 7.29 7.15C-M3, mm 6.39, 6.33 6.36, 6.24 6.57 (6.30–6.73) 6.40 (6.30–6.53) 7.00 6.54 6.86I-M3, mm 7.67, 7.38 7.26, 7.39 7.70 (7.53–8.02) 7.26 (7.14–7.39) 7.99 7.36 8.02HB, mm 9.28, 9.15 8.78, – 8.95 (8.88–9.01) 8.79, 8.81 (ns2) – – –WB, mm 10.46, 9.87 9.96, – 9.75 (9.67–9.82) 9.42, 9.65 (ns2) – – –BR, mm 6.94, 6.84 6.60, 6.39 6.64 (6.59–6.71) 6.23 (6.16–6.36) 6.87 6.48 6.74LM, mm 15.82, 15.42 14.88, 14.73 15.03 (14.60–15.54) 13.77 (12.94–14.19) 15.24 14.57 15.61HM, mm 9.01, 8.58 8.06, 7.96 8.58 (8.34–8.96) 7.79 (7.42–8.09) 8.16 8.41 8.57I-M3, mm 8.70, 8.37 8.27, 8.19 8.44 (8.11–8.67) 8.05 (7.75–8.38) 8.91 8.62 9.05

Means and ranges in parentheses are given for samples with three specimens. See the text for parameter abbreviations. *One of thespecimens was juvenile.

male and female specimens from Taiwan are: BW, 13.9 g,17 g; FA, 47.5 mm, 49.4 mm; HB, 56.0 mm, 53.2 mm;E, 16.6 mm, 15.5 mm; T, 44.4 mm, 51.6 mm; TIB,20.0 mm, 18.3 mm; and thumb, 8.5 mm, 10.0 mm. Forall specimens examined, 15 cranial measurements weretaken to the nearest 0.01 mm using digital calipers (Mit-sutoyo Co. Ltd). These included: greatest length (GTL),condylo-basal length (CBL), zygomatic breadth (ZB),interorbital constriction (IC), mastoid width (MW), palatelength (PL), width across upper molars (M3-M3), lengthfrom upper canine to last molar (C-M3), upper tooth rowlength (I-M3), height of brain (HB), breadth of braincase(BB), rostral width (RW), mandible length (M), height ofmandible (HM) and lower tooth row length (I-M3).

Chromosomal preparations of Harpiocephalus from theyoung female captured in 2003 were made from ear, tailand lung tissue cultures following Harada and Yoshida(1978). Differential stainings using the G-band and C-band techniques were applied following Seabright (1971)and Sumner (1972), respectively.

Table 1 shows the forearm length and cranial meas-urements of Harpiocephalus from Taiwan, Java (BMNH79.11.15.18, 9.1.5.356, 9.1.5.358, 9.1.5.355, 9.1.5.359,9.1.5.367), Moluccas (BMNH 45.9.18.3), Bhutan (BMNH16.7.29.42) and India (BMNH 73.4.16.4). From our meas-urements, the female has a larger body size than themale, as reported by Das (1986). Furthermore, the skullsof the male and female from Taiwan are very similar,except for some more developed features in the female,such as the crest, dentition and coronoid process of themandible (Figure 1). However, the female specimen fromTaiwan has a much broader skull with expanded zygo-matic breadth and rostral width (Table 1) and might betentatively identified as H. mordax according to the viewof Hill and Francis (1984). On the other hand, the juvenilefemale from Taiwan has intermediate skull dimensionsbetween the adult female and male specimens. This indi-cates that the characteristics existing in mordax are fea-tures in females and should be treated as the degree ofsexual dimorphism of harpia. The differences betweenthe male and female specimens from Taiwan should be

identified as the degree of sexual dimorphism and nottreated as interspecific differences between mordax andharpia as described by Corbet and Hill (1992).

The karyotype of H. harpia from Taiwan is 2ns44 andFNs52 (Figure 2A), with three large and one small met-acentric, one submetacentric, 16 medium-sized to smallpairs of acrocentric chromosomes of gradually decreas-ing size. Because no male was available, the Y chro-mosome could not be directly determined in this study.Based on the description by McBee et al. (1986) and thechromosome of Murina puta (Lin et al. 2002), whichbelongs to subfamily Murininae that includes Harpioce-phalus, the X chromosome was identified as the medium-size chromosome of a metacentric pair (Figure 2A). The



172 L.-K. Lin et al.: Updated occurrence of Harpiocephalus in Taıwan


Figure 2 Karyotypes of Harpiocephalus harpia from Taiwan. A,conventional staining; B, G-banded; and C, C-banded. Thearrow in C indicates heterochromatin in the short arm.

G-band and C-band karyotypes are given in Figure 2B,C.The karyotype of H. mordax from Thailand was reportedby McBee et al. (1986) and differs from that of H. harpiafrom Taiwan in diploid chromosome number (40 vs. 44).However, it is difficult to compare these two speciesbecause only a description is available for the karyotypeof H. mordax. Our findings on the karyotype ofH. harpia from Taiwan resemble the karyotypes of Myotisand Murina (Harada 1988; Lin et al. 2002). McBee et al.(1986) suggested that the Harpiocephalus karyotype isderived from a primitive Myotis-like karyotype and theMurina karyotype by two possible pericentric inversions.In this study, precise karyotypic data for H. harpia fromTaiwan are not shown, as mentioned above. However,additional submetacentric pairs with heterochromatin inthe short arm were observed in H. harpia from Taiwan(Figure 2C). To elucidate the taxonomic status of H. har-pia and H. mordax, molecular analyses should be per-formed in the future.

Acknowledgements

The bat survey was sponsored by a conservation grant fromCouncil of Agriculture, Taiwan, ROC. We thank Drs. H. Endo(NSMT) and P.D. Jenkins (BMNH) for permission to examinespecimens under their care. A part of the statistical analyseswere made through the facilities of the Kyoto University DataProcessing Center. We also thank Dr. Cara Lin Bridgman forrevising an early version of the manuscript.

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Updating the occurrence of Harpiocephalus harpia (Chiroptera: Vespertilionidae) and its karyology in Taiwan / Mise à jour l'occurrence de Harpiocephalus harpia (Chiroptera: Vespertilionidae)