Acta Chiropterologica, 8(1): 11–19, 2006 PL ISSN 1508-1109 © Museum and Institute of Zoology PAS

The definition of (: ) and the description of a new species from Taiwan

HAO-CHI KUO1, YIN-PING FANG2, GÁBOR CSORBA3, and LING-LING LEE1, 4

1Graduate Institute of Ecology and Evolutionary Biology, National Taiwan University, 1, Sec 4. Roosevelt Road, Taipei, Taiwan R.O.C. 2Department of Biological Resources, National Chiayi University, 300 University Road, Chiayi, Taiwan R.O.C. 3Department of Zoology, Hungarian Natural History Museum, H-1083 Budapest, Ludovika tér 2, Hungary 4Corresponding author: E-mail: [email protected]

A new species of Harpiola from Taiwan is described based on 11 specimens collected between 1998 and 2004. Careful examination of these specimens and those of the genus , revealed the valid characters distinguishing Harpiola from Murina, including the enlarged upper incisors, the well developed first premolars in both toothrows with their bulk subequal to canines and the second premolars in the corresponding toothrow, and the strongly bifid lower canine. The new species from Taiwan can be distinguished from Harpiola grisea in India by having different shape of second upper premolar and different structure of first upper molar.

Key words: Harpiola sp. nov., Taiwan,

INTRODUCTION The description of the genus Harpiola was based on a single specimen collected Within the subfamily Murininae two from Northwest India and both the wet genera are accepted generally, namely specimen and its extracted skull are in Murina and Harpiocephalus (Corbet and a very bad condition. As Corbet and Hill Hill, 1992; Koopman, 1993, 1994; Pav- (1992: 151) stated “the features upon which linov, 2003; Simmons, 2005). The name Thomas based Harpiola do not appear to be Harpiola was introduced by Thomas (1915) artificial, but to some extent the status of as a separate genus with Murina grisea grisea must remain uncertain until further Peters, 1872 as its type species. Although material is obtained.” Recently, alongside Tate (1941) accepted this opinion and pro- the description of the second known speci- vided a brief diagnosis of the genus (char- men of H. grisea from Mizoram, India, acterized by the attachment point of the Bhattacharyya (2002) re-evaluated Har- wing and by dental features), Ellerman piola and raised once again the taxon to and Morrison-Scott (1951) listed this form generic rank. as a subgenus of Murina, a taxonomic During a series of surveys carried arrangement which was followed subse- out between 1998 and 2004 in mountain quently. areas in Taiwan, 11 Harpiola were 12 H.-C. Kuo, Y.-P. Fang, G. Csorba, and L.-L. Lee obtained that contributed to the richest col- — taken across the outer borders of upper canines; lection of specimens of this genus in the upper molar width — taken across the outer crowns of world. In this paper, detailed comparisons the last upper molars; zygomatic width — the great- est width of the skull across the zygomatic arches; of these specimens with those of H. grisea mastoid width — the greatest distance accross the and Murina spp. were made to reveal their mastoid region; postorbital width — the least width of taxonomic status and to re-define the diag- the postorbital constriction; maxillary toothrow nostic features of the genus Harpiola. length — from the front of upper canine to the back Meanwhile, the special zoogeography of of the crown of the third molar; upper canine–premo- Harpiola as well as other mammalian gen- lar length — the largest distance from the front of the upper canine to the back of the crown of the posterior era was also considered. premolar; length of mandible — from the anterior rim of the alveolus of the first lower incisor to the most MATERIALS AND METHODS posterior part of the condyle; mandibular toothrow length — from the front of the lower canine to the The following comparative material was used: back of the crown of the third lower molar; lower ca- Harpiola grisea: India, BM(NH) 79.11.21.117 (holo- nine–premolar length — the greatest distance from type); Murina aenea: Malaysia, BM(NH) 64.770 the front of the lower canine to the back of the crown (holotype); M. aurata: China, MNHN CG1870-590a of the posterior premolar; height of the coronoid (paratype); M. cyclotis cyclotis: India, BM(NH) process — taken perpendicularly from the extremity 9.4.4.4 (cotype); M. cyclotis peninsularis: Malaysia, of the coronoid process to the ramus mandibulae. BM(NH) 64.771 (holotype); M. florium: Indonesia, BM(NH) 63.12.26.14 (holotype); M. hilgendorfi: Ja- pan, HZM 1.2974; M. huttoni: India, BM(NH) EVALUATION OF THE HARPIOLA CHARACTERS 79.11.21.685 (holotype); M. leucogaster rubex: India, BM(NH) 16.3.25.111 (holotype); M. puta: Taiwan, One of the main diagnostic features at- ZMNTU 1998.7.3; M. rozendaali: Malaysia, tributed to Harpiola is the attachment point BM(NH) 83.360 (holotype); M. silvatica: Japan, of the plagiopatagium. According to Tate HNHM 2001.38.1; M. suilla: Java, HNHM 2000.13.2; M. tubinaris: Pakistan, HNHM 99.14.6; (1941), Corbet and Hill (1992), Koopman M. ussuriensis: Russian Federation, ZMMU 96368 (1994), and Bhattacharyya (2002), it is at- (paralectotype). tached to the base of the first toe in Harpio- The museum acronyms mentioned in the text are la whereas it is attached to the base of the as follows: BM(NH) — Natural History Museum, claw of the first digit (the distal phalanx) in London, formerly British Museum (Natural History); ESRI — Endemic Species Research Institute, Nan- Murina. However, when describing M. hil- tou; HNHM — Hungarian Natural History Museum, gendorfi, Peters (1880) noted and figured Budapest; HZM — Harrison Institute, Sevenoaks, the attachment of the wing as being close to formerly Harrison Zoological Museum; MNHN — the base of the first toe. This view was sup- Museum National d’Histoire Naturelle, Paris; NMNS ported subsequently by Wallin (1969) and — National Museum of Natural Science, Taichung; ZMNTU — Zoological Museum of National Taiwan Yoshiyuki (1989). The latter described the University, Taipei; THU — Tunghai University, Tai- Japanese population of M. hilgendorfi as chung; ZMMU — Zoological Museum of Moscow having a “plagiopatagium attached to basal State University, Moscow. portion of first phalanxes of the first toe” The forearm (FA) measurements were taken from (Yoshiyuki, 1989: 216). Ognev (1928) not- dry or alcohol preserved museum specimens with 0.1 mm accuracy. The following craniodental measure- ed a similar point of attachment for M. og- ments were taken to the nearest 0.01 mm by the au- nevi and M. sibirica (these latter taxa are thors with digital calipers under a stereomicroscope: considered to be synonyms of M. hilgen- total length of skull — from the anterior rim of alve- dorfi — see Simmons, 2005). However, this olus of the first upper incisor to the most projecting point of the occipital region; condylobasal length — character was overlooked by subsequent au- from the exoccipital condyle to the posterior rim of thors and curiously Tate (1941: 579, 580), alveolus of the first upper incisor; upper canine width although citing Ognev’s (1928) statements, A new species of Harpiola from Taiwan 13 erroneously listed the attachment point as in M. aurata. In conclusion, the degree of a differentiating character of Harpiola. reduction of canines in both upper and low- For dental characters, the main distin- er toothrows can not serve as diagnostic guishing feature of Harpiola cited by Tate characters distinguishing Harpiola from (1941), Corbet and Hill (1992), and Koop- Murina. man (1994) was the reduction of the meta- The characters of Harpiola (Figs. 1 and cones of the anterior and middle upper 2) which do support its generic distinction molars. However, these authors were only are: 1) the upper incisors (I2 and I3) are ap- able to investigate the holotype of H. grisea proximately two-third that of the C1 in (the single known specimen of the genus at height; the basal area of second upper inci- that time) the teeth of which are extremely sor (I3) is more than two-third that of C1 (in worn. Bhattacharyya (2002) in his descrip- Murina, the height and crown area of I2 and tion of a second specimen of this species did I3 are at most half that of the C1); 2) the not mention the cusp pattern of the molars. basal area of C1, P2 and P4 are subequal, Nevertheless, in Harpiola from Taiwan (de- their height are gradually decreasing; the scribed herein as new species), the meta- corresponding teeth are similar in bulk and cones of the first (M1) and second (M2) mo- height in the lower toothrow (in Murina the lars are well developed and clearly higher canine always greatly exceeds the first pre- than the paracones. Furthermore, Thomas molar in height in both toothrows; P2 almost (1915), Corbet and Hill (1992), and Bhat- always, clearly smaller than P4 in height); 3) tacharyya (2002) all mentioned the high- C1 is strongly bifid, and the additional cusp ly reduced canines of Harpiola, which are is well developed (in Murina only a small in contrast with the usual specialized ca- secondary cingular cusp is present). These nines seen in Murina. However, even high- diagnostic characters can also be seen in er degree of reduction in the bulk of upper the type of H. grisea; however, the cusp canine can be observed in M. aurata (Mae- structure of C1 can hardly be detected due to da, 1980; Corbet and Hill, 1992). Although the very bad condition of the specimen. quantitative comparison and statistical analysis were not applicable because very SYSTEMATIC DESCRIPTION few specimens of relevant species are avail- able in the museum collections, detailed Harpiola isodon sp. nov. examination of comparative material in this study revealed that the upper canine of Holotype the new species from Taiwan is clearly the ZMNTU 1998.5.3, adult Y, dry skin and highest one in the upper toothrow with the skull. Collected by T. S. Ding and K. Y. basal area subequal to that of the second Wang on 2 May 1998. premolar, and is not especially reduced as compared to those of M. aurata. As for Type locality lower canine, the new species of Harpio- Hualien County, Jhuosi Township, Yu- la from Taiwan shows higher degree of re- li Wildlife Refuge, 23°32’N, 121°15’E, duction in both bulk and height than most 2,000 m a.s.l. species of genus Murina except M. aurata. The new species of Harpiola from Taiwan Paratypes has both basal area and height of lower ESRI B0358, adult X, in alcohol, skull canine subequal to those of lower second extracted, Taichung County, Tahsuehshan premolar, similar proportions are also found Forest Recreation Area, Tahsuehshan #210 14 H.-C. Kuo, Y.-P. Fang, G. Csorba, and L.-L. Lee logging road, 1,950 m a.s.l.; ESRI B0359, 2004.19.13. adult Y, skin and skull, Taitung adult X, dry skin and skull, Taichung Coun- County, Taimali Township, E-ma logging ty, Tahsuehshan Forest Recreation Area, road, 22°37’N, 120°56’E, 1,000 m a.s.l.; Tahsuehshan #210 logging road, 1,950 m HNHM 2004. 19.15, adult X, skin and a.s.l.; THU B050016, adult Y, dry skin and skull, Chiayi County, Alishan Forest Re- skull, Chiayi County, Alishan Township, creation Area, Sister Ponds, 23°31’N, Lulinshan Major Wildlife Habitats, 2,400 m 120°48’E, 2,200 m a.s.l. a.s.l.; ZMNTU 2003.8.4, adult X, dry skin and skull, Ilan County, Nanau Township, Etymology Nanaunan logging road, 1,000 m a.s.l.; The name isodon (‘equal-toothed’ in NMNS 4858, adult X, dry skin and skull, English) refers to the subequal basal area of Taichung County, Heping Township, Wul- the canines, first and second premolars typ- ing Farm; NMNS 5741, adult Y, in alcohol, ical for the genus. skull extracted, Nantou County, Renai Township, Tsueifong; THU 7385, adult Y, Diagnosis dry skin and skull, Chiayi County, Alishan This is a medium-sized tube-nosed bat Township, Lulinshan Major Wildlife Habi- with the forearm length between 31–36 mm tats, 2,400 m a.s.l.; HNHM 2003.36.31, (Table 1). Guard hairs of dorsal fur are adult X, in alcohol, skull extracted, Nantou with shiny bright golden tips; the uropata- County, Renai Township, Meifong Farm, gium is densely furred on both sides; wing 24°06’N, 121°11’E, 2,100 m a.s.l.; HNHM membrane is attached at the base of first toe.

A

B

FIG. 1. Lateral views of skulls of: A — Harpiola isodon sp. nov. (paratype HNHM 2003.36.31.) from Taiwan; B — Murina suilla (type species of the genus, HNHM 2000.13.2.) from Java. Scale = 5 mm A new species of Harpiola from Taiwan 15

The basal area of canines and the premolars of the individual hair of underfur is dark are subequal in both toothrows; P4 is wider brown with a bright yellow subterminal than long; mesostyles of M1 and M2 are less band and a dark brown tip. Guard hairs developed but usually visible, the first up- scattered all over the back (including the per molar is with a more or less developed flanks and the nape) are dark brown in basal postcingular platform. four-fifths and with shiny golden yellow tips. The general colouration of back is Description thus extremely similar to that of M. aurata The fur on the back is very long (9–10 being described as “rich mixture of gold and brown” (Bates and Harrison, 1997: mm in length, some guard hair can be as 204). The dorsal side of the tail membrane, long as 14 mm) and woolly; the basal part the tibia and the foot are all densely and evenly furred including the last caudal ver- A tebra which is free from the uropatagium. The whole length of the forearm, the thumb and even the proximal part of the fifth metacarpal are covered with short golden coloured fur (Fig. 3). In ventral aspect the fur is shorter, dark brown at the base and light brown in the terminal one-third. Some individuals have greyish white hairs pre- dominated along the midline of chest and abdomen. The whole area of the tail mem- brane is also covered with dense, stiff, sil- very grey hairs. The ear is 12.5–13.0 mm in length, the ear conch is rounded with a very distinct emargination at the upper third of its posterior border; the tragus is medium long (6.5–8.0 mm) but wide at its base and B gradually tapering to the backward-curved tip which just reaches the level of the notch; the base of tragus is with a small tooth-like projection at its outer margin. The skull is delicately built, the brain- case is moderately bulbous, rostral profile is evenly ascending. There is no sagittal crest, the lambdoid crest is medium developed (Fig. 1A). The narial emargination is much C longer than wide; there is no basioccipital fissure. Basioccipitale is with well-defined basial pits. The zygomatic arch is weak and slender, almost parallel-sided. FIG. 2. A — Occlusal view of left upper dentition; The inner upper incisor (I2) is anterior B — lateral view of right mandible; and C — lingual view of left lower I , C and P teeth of H. isodon sp. to and only very little longer than the outer 3 1 2 3 nov. (paratype, HNHM 2003.36.31.) from Taiwan. upper incisor (I ). Both upper incisors Scales for A and B = 5 mm, and for C = 1 mm are about two-third that of the C1 in height; 16 H.-C. Kuo, Y.-P. Fang, G. Csorba, and L.-L. Lee

TABLE 1. Selected external and craniodental measurements of H. isodon sp. nov. (in mm) Paratypes Parameter Holotype n min–max Forearm length 31.40 9 31.00–35.60 Total length of skull 15.50 10 14.76–16.48 Condylobasal length 13.87 10 13.74–14.87 Upper canine width 3.65 10 3.65–4.02 Upper molar width 5.17 10 4.90–5.53 Zygomatic width 8.92 10 8.43–9.35 Mastoid width 7.36 10 7.29–7.96 Postorbital width 4.51 10 4.52–4.84 Maxillary toothrow length 4.98 10 4.97–5.63 Upper canine–premolar length 2.34 10 2.22–2.73 Length of mandible 10.28 10 10.15–11.32 Mandibular toothrow length 5.28 10 5.35–5.90 Lower canine–premolar length 2.14 10 2.02–2.44 Height of the coronoid process 3.48 10 3.36–3.98 the basal area of second upper incisor is premolar is wider than long, M1 and M2 are more than two-third that of C1 (Fig. 2A). usually with very small but recognizable The basal area of C1, P2 and P4 are sube- mesostyle, the first upper molar is with a qual, their height are gradually decreasing. definite postcingular platform. The metacones of M1 and M2 are distinctly The mandible is slender, the corpus higher than the paracones. Second upper mandibulae is delicate; the symphysis is

FIG. 3. Photo of a living individual of H. isodon sp. nov. (paratype, ESRI B0358) A new species of Harpiola from Taiwan 17 long and procumbent, protruding anterior- from H. isodon sp. nov. in having a rela- ly; there is a distinct indentation in the cor- tively narrow second upper premolar which pus in front of the angular process. The is almost as long as wide; M1 is with no coronoid process is low (Fig. 2B). The low- postcingular platform and M2 is without er canine has a well developed additional any trace of mesostyle (Fig. 4) which is cusp (Fig. 2C); C1 and premolar teeth are usually weak but present in H. isodon. similar in both bulk and height among which C1 is slightly less in height and P2 is Natural history smaller in basal area. The entoconid of M1 Individuals were sporadically captured and M2 is lower than the hypoconid but has in mountain areas with elevations between a distinct cusp and is widely separated from 1,000 and 2,400 m a.s.l. in Taiwan. They the metaconid; therefore a clear posterior occurred mostly in coniferous plantations trigonid is present. or mixed forests of coniferous and broad- leaf trees with more or less closed canopy. Comparisons Two of them were found in a tunnel. One Harpiola grisea, the only other species female (ESRI B0358), which was caught in in the genus with only one specimen before May, 2002 had one fetus. Bhattacharyya (2002), is described by Hut- ton (1872: 712) as “colour above grey Zoogeography mouse-brown, beneath paler grey.” It is the Although Taiwan belongs to the Indo- same specimen, however, described by malayan zoogeographical region, in the Dobson (1876: 154) as “fur, above, dark first compilation of the fauna of brown with yellowish brown extremities; the island Kuroda (1952: 285) emphasize beneath, similar, but the extreme points of the fact that “Formosa […] has rich ele- the hairs are rather ashy”, which is closer to ments of the Palaearctic or the Himalayan our observation. The external distinction on the mountainous parts”. The systematic between H. grisea and H. isodon sp. nov. in and taxonomic composition of Taiwanese Taiwan seems to be the colour of extremi- mammalian fauna has changed a lot in the ties of dorsal hairs, which is dark brown light of the recent studies, but there are (underfur) or shining golden yellow (guard some examples among volant and non- hairs) in the latter taxon. Interestingly, volant mammal groups which occur only Bhattacharyya (2002) observed the Mizo- in Taiwan and in the high mountains of ram specimen as having hairs on the dor- sum with shining golden yellow tips, strik- AB ingly similar to those of H. isodon. Further materials of H. grisea, especially from sites that are close to the type locality, are still needed to make clear the range of variation in pelage colouration of this unique species, or that the Mizoram specimen actually rep- resents a separate taxon. The condition of the H. grisea holotype skull makes any detailed morphological FIG. 4. Occlusal view of the left P4, M1 and M2 teeth of: A — H. isodon sp. nov. (paratype, HNHM 2003. investigation and measuring impossible, 36.31.) from Taiwan and B — H. grisea (holotype, and only the shape and size of teeth can be BM(NH) 79.11.21.117) from Uttar Pradesh, India. compared. Harpiola grisea differs dentally Scale = 3 mm 18 H.-C. Kuo, Y.-P. Fang, G. Csorba, and L.-L. Lee mainland Asia. This kind of connection is in the collection of the Indian Museum, Cal- supported by the distribution patterns of cutta. Trustees of the Indian Museum, London, shrews (Soriculus and Chodsigoa spp. — 228 pp. ELLERMAN, J. R., and T. C. S. MORRISON-SCOTT. 1951. see Motokawa et al., 1997), mole-shrews Checklist of Palaearctic and Indian (Anourosorex squamipes and A. yamashinai 1758 to 1946. Trustees of the British Museum — see Motokawa and Lin, 2002; Motokawa (Natural History), London, 810 pp. et al., 2004), vesper bats (Arielulus aureo- HUTTON, T. 1872. On the bats of the north-western collaris and A. torquatus — see Csorba and Himalayas with notes and corrections in no- menclature by W. Peters, C.M.Z.S. Proceedings Lee, 1999) and voles (Volemys spp.). The of the Zoological Society of London, 1872: species-pair of H. isodon and H. grisea is 690–714. an important addition to this list. KOOPMAN, K. F. 1993. Order Chiroptera. Pp. 137–241, in Mammal species of the word: a taxonomic and geographic reference. 2nd edition (D. E. WILSON ACKNOWLEDGEMENTS and D. M. REEDER, eds.). Smithsonian Institution Press, Washington D.C., 1206 pp. We are very grateful to Hsi-Chi Cheng (Endem- KOOPMAN, K. F. 1994. Chiroptera: systematics. Hand- ic Species Research Institute, Chichi), Yen-Jean Chen book of Zoology. Mammalia, part 60. Walter de (National Museum of Natural Science, Taichung), Gruyter, Berlin, 217 pp. Liang-Kong Lin (Tunghai University, Taichung), KURODA, N. 1952. Mammalogical history of Formo- Paula Jenkins (Natural History Museum, London), sa, with zoogeography and bibliography. Quar- Jacques Cuisin (Muséum National d’Histoire Natur- terly Journal of Taiwan Museum, 5: 267–304. elle, Paris) and Paul J. J. Bates (Harrison Institute, MAEDA, K. 1980. Review on the classification of lit- Sevenoaks) who kindly provided access to the speci- tle tube-nosed bats, Murina aurata, group. Mam- mens under their care. György Topál help us with his malia, 44: 531–551. expert advice and by the preparation of some speci- MOTOKAWA, M., and L.-K. LIN. 2002. Geographic mens. The work of HCK, YPF, and LLL was sup- variation in the mole-shrew Anourosorex squa- ported by the Nature Conservation Grant of the mipes. Mammal Study, 27: 113–120. Council of Agriculture, Taiwan, ROC. The work of MOTOKAWA, M., H.-T. YU, Y.-P. FANG, H.-C. CHENG, GCS was supported by the European Commission’s L.-K. LIN, and M. HARADA. 1997. Re-evaluation Research Infrastructure Action via the SYNTHESYS of the status of Chodsigoa sodalis Thomas, 1913 Project. (Mammalia: Insectivora: Soricidae). Zoological Studies, 36: 42–47. LITERATURE CITED MOTOKAWA, M., M. HARADA, L.-K. LIN and Y. WU. 2004. Geographic differences in karyotypes of BATES, P. J. J., and D. L. HARRISON. 1997. Bats of the the mole-shrew Anourosorex squamipes (Inse- Indian subcontinent. Harrisson Zoological Muse- ctivora, Soricidae). Mammalian Biology, 69: um Publication, Sevenoaks, 258 pp. 197–201. BHATTACHARYYA, T. P. 2002. Taxonomic status of the OGNEV, S. I. 1928. Mammals of Eastern Europe and genus Harpiola Thomas, 1915 (Mammalia: Chi- Northern Asia. Volume 1. Insectivora and Chiro- roptera: Vespertilionidae), with a report of the oc- ptera. Glavnauka, Moscow, 631 pp. [in Russian]. currence of Harpiola grisea (Peters, 1872) in Mi- PAVLINOV, I. Y. 2003. Systematics of recent mam- zoram, India. Proceedings of the Zoological So- mals. Moscow University Publisher, Moscow, ciety, Calcutta, 55: 73–76. 296 pp. [in Russian]. CORBET, G. B., and J. E. HILL. 1992. The mammals of PETERS, W. 1880. Mittheilung über die von Hrn. Dr. the Indomalayan region. Natural History Muse- F. Hilgendorf in Japan gesammelten Chiropteren. um and Oxford University Press, Oxford, 488 pp. Monatsberichte der Königlich Preussischen Aka- CSORBA, G., and L.-L. LEE. 1999. A new species of demie der Wissenschaften, 1880: 23–25. vespertilionid bats from Taiwan and a revision of SIMMONS, N. B. 2005. Order Chiroptera. Pp. the taxonomic status of Arielulus and Thainycte- 312–529, in Mammal species of the Word: a tax- ris (Chiroptera: Vespertilionidae). Journal of Zo- onomic and geographic reference. 3rd edition ology (London), 248: 361–367. (D. E. WILSON and D. M. REEDER, eds.). The DOBSON, G. E. 1876. Monograph of the Asiatic Johns Hopkins University Press, Baltimore, Chiroptera, and catalogue of the species of bats 2142 pp. A new species of Harpiola from Taiwan 19

TATE, G. H. H. 1941. Results of the Archbold ex- bat known as Murina grisea. Annals and Maga- peditions no. 40. Notes on Vespertilionid bats of zines of Natural History, 8, 16: 309–310. the subfamilies Miniopterinae, Murininae, Ke- WALLIN, L. 1969. The Japanese bat fauna. Zoologiska rivoulinae and Nyctophilinae. Bulletin of the Bidrag frDn Uppsala, 37: 223–440. American Museum of Natural History, 78: YOSHIYUKI, M. 1989. A systematic study of the Japa- 567–597. nese Chiroptera. National Science Museum, THOMAS, O. 1915. A special genus for the Himalayan Tokyo, 242 pp.

Received 02 September 2005, accepted 10 December 2005