New findings and an extensive description of Rhinolophus marshalli Thonglongya, 1973 in Vietnam

Citings of Marshall’s horseshoe bat in areas where it has been previously found have been rare. Prior to this study, little was known about this species. By making use of data and material that were obtained in a series of field surveys conducted between 2006 and 2011, this paper provides an extensive view of the species and presents new findings important to future systematic studies and conservation assessments.

JOURNAL OF SCIENCE OF HNUE Chemical and Biological Sci., 2012, Vol 57, No 8, pp 90-97 This paper is available online at http://stdb.hnue.edu.vn NEW FINDINGS AND AN EXTENSIVE DESCRIPTION OF Rhinolophus marshalli THONGLONGYA, 1973 IN VIETNAM Vu Dinh Thong Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology Abstract Marshall’s horseshoe bat, Rhinolophus marshalli was first discovered in Thailand and was recorded in Vietnam in 1973 Over the past thirty-nine years, populations of this species have been found in China, Myanmar, Vietnam, Lao PDR, Thailand and Malaysia Citings of Marshall’s horseshoe bat in areas where it has been previously found have been rare Prior to this study, little was known about this species By making use of data and material that were obtained in a series of field surveys conducted between 2006 and 2011, this paper provides an extensive view of the species and presents new findings important to future systematic studies and conservation assessments Keywords: Asia, echolocation, ecology, Mammalia, Rhinolophidae, taxonomy Introduction To date, a total of eighty-five species of Rhinolophus have been identified in the old world [3, 7, 10] Of these, Marshall’s horseshoe bat, Rhinolophus marshalli, was discovered and described in Thailand by Thonglongya [6] Due to the dearth of additional citings, it is considered to be one of the rarest horseshoe bat species in Asia Bates et al [1] noted that “it is always found as individuals, never in large numbers.” However, this study postulates that Marshall’s horseshoe bat lives in colonies that consist of large numbers of individuals Little is known about this species or the true extent of its distribution range With reference to materials and data obtained from recent investigations, this paper provides a comprehensive view that includes new findings of Marshall’s horseshoe bat for taxonomic identification and conservation assessment Received November 2, 2012 Accepted November 23, 2012 Biology Subject Classification: 10 612 Contact Vu Dinh Thong, e-mail address: thong@iebr.ac.vn 90 New findings and an extensive description of Rhinolophus marshalli Thonglongya 2.1 Content Material and methods 2.1.1 Bat capture Field surveys were carried out in a number of protected areas of Vietnam, which included national parks and nature reserves, between March 2006 and December 2011 Four-bank harp traps and mist nets of various sizes were employed to capture bats Each captured bat was carefully removed from the trap or net and placed individually in a cotton bag 2.1.2 Materials and morphometric measurements The acronym IEBR-T refers to Vu Dinh Thong collection which is now retained at the Institute of Ecology and Biological Resources (IEBR), Hanoi, Vietnam Morphormetric measurements were taken from sixteen live individuals and voucher specimens The voucher specimens are identified as IEBR-T.271107.1 (male), in alcohol, skull removed, collected on November 27, 2007, Binh Thuan Area, Phong Lai Commune, Thuan Chau District, Son La Province, no co-ordinate; IEBR-T.090108.2 (male), collected on January 9, 2008, skull removed; IEBR-T.070909.1 (female), collected on September 7, 2009; IEBR-T.090909.1 (male), collected on September 9, 2009, the last two both in alcohol, skulls remain, Cat Ba National Park, Hai Phong, 20◦ 47’N, 106◦ 59’E, 38 m a.s.l The following external and craniodental measurements were taken using a digital caliper to the nearest 0.1 mm FA, forearm length; EH, ear height; EW, ear width; TIB, tibia length; HF, hind-foot length; T, tail length; 3rdF, total length of the third digit; 4thF, total length of the fourth digit; 5thF, total length of the fifth digit; SL, total length of skull; CCL, condylocanine length; IOW, interorbital width; ZW, zygomatic width; MW, mastoid width; C1 - C1, upper canine width; M3 - M3, upper molar width; C1 - M3, maxillary toothrow length; ml, mandible length; c1 - m3, mandibular toothrow length; TBL, total bacular length; GWB, greatest width at the base of the baculum; GWM, greatest width at the mid-point of the shaft of the baculum; GWT, greatest width at the bacular tip The above measurements are illustrated in Bates and Harrison [2] and Csorba et al [3] Reproductive status and age were assessed following Racey [5] Body mass (BM) ) measurement was taken in the field within hour after capture using a 50 g LightLine Spring balance To reduce the influence of seasonal variations in body mass, juveniles and pregnant females were excluded from analyses 2.1.3 Recording and analysis of echolocation signals Echolocation calls were recorded inside a flight-tent using a PCTape system at a sampling rate of 480 kHz Batman software, which displays color sonagrams of 91 Vu Dinh Thong the detected echolocation signals in real time, was used to obtain high quality sound sequences Additionally, continuous recordings were made in front of caves and under forest canopies to obtain echolocation calls when bats were leaving their roosts and foraging in their natural habitat, respectively All echolocation signals obtained from manual and continuous recordings were analysed using Selena software to measure the constant frequency component of the second harmonic (CF2) of each call The PCTape system and the Batman and Selena software were custom-made by the University of Tăubingen, Germany 2.2 Results and discussion * External characters Rhinolophus marshalli is a medium-sized horseshoe bat species, with a forearm length and ear height of 43.0 - 48.3 mm (n = 20) and 23.0 - 27.5 mm (n = 20), respectively (Table 1) The pelage of this species varies between light and dark-brown The hair tip, around one-fourth of a hair length, is distinctly darker than the rest of the hair The anterior leaf has a narrow, deep emargination and covers the upper lip (Figure 1) The internarial region greatly expends covering the nostrils from the above view Its edges raise and connect to the sella base to form a cup-like structure The sella is large, broad and stands vertically upon the cup Its height is slightly larger than its width The upper margin of the sella is rounded while the lateral margins are slightly concave The connecting process is low and rounded The posterior leaf is low and hidden by the sella in a frontal view The ears are quite large, extending far beyond the muzzle when laid forward The antitragus is large with a broadly rounded tip Its height equals approximately half the respective EH Long hairs sparsely cover the anterior face of the lancet and the upper lip There are three vertical grooves on the lower lip Tail length is in range of 22.0 - 27.0 mm The wing attaches at the toe base The metacarpals are nearly equal in length (Table 1) Figure Frontal (a), lateral (b) and horizontal (c) views of the face and ear of R marshalli 92 New findings and an extensive description of Rhinolophus marshalli Thonglongya Table Morphological, bacular and craniodental measurements of Rhinolophus marshalli Measurements Range n FA 43.0 - 48.3 20 EH 23.0 - 27.5 20 TIB 17.5 - 20.8 20 HF 6.0 - 8.6 20 T 22.0 - 27.0 20 3rdF 64.0 - 69.5 20 4thF 51.0 - 56.0 20 5thF 52.0 - 60.0 20 TBL 4.0 - 4.2 GWB 1.1 - 1.3 GWM 0.2 - 0.3 GWT 0.2 - 0.4 SL 18.0 - 19.0 CCL 16.1 - 16.8 IOW 2.3 - 2.6 ZW 8.3 - 8.6 MW 9.2 - 9.4 C1 - C1 3.8 - 4.0 M3 - M3 5.6 - 6.0 C1 - M3 6.4 - 6.6 ML 11.2 - 12.0 c - m3 6.8 - 7.5 * Craniodental characters The skull is rather long and slender with a maximum length of 18.0 - 19.0 mm (Figure and Table 1) The mastoid width is always larger than that of the zygoma The sagittal crest is very low connecting to the unsharp supra-orbital crest The zygoma are thin, slightly curved upward The cochleae are large with very narrow basioccipitals The upper incisors are minute and bifid Both upper canine and posterior upper premolars (P3 ) are developed The first upper premolar (P2 ) is small, stands in the tooth-row and is separated from the two adjacent teeth The first upper molar (M1 ) is slightly higher than the second (M2 ) and third (M3 ) The lower incisors are minute and bifid The second lower premolar (P3 ) is small, situated in the tooth-row 93 Vu Dinh Thong Figure Dorsal, ventral, and lateral (from top-left clockwise) views of the skull and mandible of Rhinolophus marshalli (IEBR-T.271107.1) Scale = mm * Bacular morphology The baculum is small with a total length of 4.0 - 4.2 mm (Figure and Table 1) There is a deep hollow in the base with expanded margins The proximal margin of the base is elongated in lateral view The ventral emargination on the proximal margin is rather deep and narrow, but on the dorsal side it is shallow and wide The dorsal knob is distinct There is a vertical groove at the base in the ventral view The shaft bends slightly dorsally The tip is unusually expanded, forming a circular ‘plate-like’ structure with an uneven surface * Echolocation Echolocation calls of this species are typical of other species of the genus Rhinolophus Each signal consists of three distinct portions: an initial modulated frequency, constant frequency and the terminal modulated frequency Its CF2 is in a range of 42.0 - 45.4 kHz (n = 15) In its natural habitat, Rhinolophus marshalli emits long single signals whilst searching, and a number of short signal groups when reacting to/upon an object or a prey * Habitats Rhinolophus marshalli has been recorded in both primary and secondary forests 94 New findings and an extensive description of Rhinolophus marshalli Thonglongya of limestone areas in northern and central Vietnam On Cat Ba island, two individuals were collected at a garden in which was growing litchi, jack-fruit, banana and other bush species Additional individuals were captured on this island in secondary forest habitat within limestone karst zones Rhinolophus marshalli cohabits with Aselliscus stoliczkanus, Hypsugo cf pulveratus and Hipposideros armiger The species Cynopterus sphinx, Hipposideros alongensis alongensis, Hipposideros cf grandis, Hipposideros pomona and Rhinolophus affinis were recorded within the foraging areas of Rhinolophus marshalli Figure Lateral (left), ventral (central), and dorsal (right) views of the bacula of R marshalli (IEBR-T.090108.2) Scale = mm * Reproduction and colony size A pregnant Rhinolophus marshalli female was collected on April 12, 2007 in Ca Ba National Park The record suggests that this individual would give birth in May This record provides the first data on reproduction of Rhinolophus marshalli Colonies of up to eleven individuals in Cat Ba National Park and six individuals in Xuan Son National Park were captured during this study * Taxonomic and acoustic remarks Rhinolophus marshalli is one of the smallest species of the “philippinensis-group” [3, 10] All obtained materials refer to the nominate form The horseshoe and sella of this species represent typical structures of the philippinensis-group They are similar 95 Vu Dinh Thong to those of R paradoxolophus in shape, but distinctly smaller in size To date, the philippinensis-group comprises ten taxa: Rhinolophus huananus, R macrotis [large form], R macrotis [small form], R marshalli, R montanus, R paradoxolophus, R philippinensis, R rex, R schnitzleri and R siamensis [10] Of these, R marshalli is distinguishable from the others in external and bacular morphology Its bacular size is almost equal to that of R rex, greater than that of R macrotis [small form], and smaller than all others of the species [10, Figure 3] Vu Dinh Thong et al [9] provided the first data on echolocation of this species from Vietnam with CF2 value of 44.0 kHz Results from this study indicate that the CF2 value of this species ranges between 42.0 and 45.4 kHz * Distribution The species has been known from China, Myanmar, Vietnam, Lao PDR, Thailand, and Malaysia [1, 3] It was first recorded in Vietnam by Hill and Topal [4] This species was also recorded Sa Pa area, Lao Cai Province [3] and Hoi An area, Quang Nam Province (Glenn Hoye, pers.comm.) * Habitat and conservation status The habitat of Rhinolophus marshalli is typically a dry, deciduous forest covering foothills that are close to rice fields [6] It has been found mostly in limestone karst habitat [3, 8] Marshall’s Horseshoe Bat is listed as “Least Concern” in the 2011 IUCN Red List of Threatened Species [1] No strategy has been made for the conservation of this species within its distribution range Protection of the caves in Vietnam, where this species is living, is highly recommended and appropriate with reference to the information presented in this study Conclusion Marshall’s horseshoe bat (Rhinolophus marshalli) is distinguishable from other horseshoe bat species by its morphological, craniodental, bacular and acoustic features Rhinolophus marshalli is distributed and forages within both primary and secondary forests that are in or close to karst areas Rhinolophus marshalli uses echolocation calls with a CF2 of 42.0 - 45.4 kHz Its calls represent typical signals of the genus Rhinolophus Rhinolophus marshalli mostly inhabits caves and lives in colonies of up to eleven individuals 96 New findings and an extensive description of Rhinolophus marshalli Thonglongya REFERENCES [1] Bates P., Francis C., Csorba G., 2008 Rhinolophus marshalli In: IUCN 2011 IUCN Red List of Threatened Species Version 2011.2