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New findings of the white-toothed shrews (Crocidura spp.) from offshore islands of Vietnam are reported. The species identifications have been confirmed by the analysis of complete mitochondrial cytochrome b gene (1140 bp). Crocidura phuquocensis is the only species found in the Phu Quoc Island. Crocidura fuliginosa has been recorded from two islands of the Con Dao Archipelago (Con Son and Bai Canh). The occurrence of Crocidura fuliginosa in Vietnam has been genetically confirmed for the first time. Crocidura attenuata has been collected from the Cat Ba Island for the first time, and this finding corresponds well with the proposal that the species’ distribution is confined to the north and east of the Red River only.
Crocidura fuliginosa, Crocidura attenuata, Crocidura phuquocensis, biogeography, Cat Ba, Con Dao, Phu Quoc, SE Asia
Biodiversity of Southeast Asian islands has often been the focus of intensive studies by systematists, evolutionary biologists and biogeographers (
Despite its small size, Vietnam has a very long coastline (near 3500 km) and is surrounded by more than 3000 islands. The majority of Vietnamese coastal islands are situated within a shallow shelf. Two main stages of the geological history of this area can be recognized (
Most mammal surveys of Vietnamese islands have been devoted to the study of rodents and large mammals (
Phu Quoc is the largest Vietnamese island (it covers ca. 562 km2) lying in the Gulf of Thailand, ca. 15 km south of the coast of mainland Cambodia. Primary lowland tropical forests still cover the northeastern part of the island. The first mammalogical survey of Phu Quoc was carried out of the VRTC (
The Con Dao Archipelago is situated in the monsoon belt of the South China Sea at about 90 km off mainland Vietnam. Con Son, formerly known as Pulo Condor, consists of the largest (ca. 52 km2) island of archipelago, surrounded by 14 smaller islets. The topography of Con Son Island is mountainous, and is dominated by the granite ridge running from south-west to north-east and is covered by primary tropical forest. A biodiversity survey of Con Son was conducted by the VRTC from 26 May to 12 June, 2010. Small mammal trapping was conducted using plastic buckets (25×20 cm) and glasses (13×9 cm) as pitfall traps. Trapping took place for a total of 1237 trap-nights, distributed unequally between 13 survey sites.
Cat Ba is the largest of hundreds of islands that comprise the Cat Ba Archipelago and is located at the southeastern edge of Ha Long Bay in northern Vietnam. Cat Ba Island lies approximately 30 km east of Hai Phong city in northern Vietnam and has a surface area of 285 km2. The landscape of Cat Ba is dominated by limestone karst with alternating narrow valleys running along the northeast-southwest line. The main natural vegetation type on Cat Ba consists of moist tropical forest on limestone karst, however, in large areas it is now replaced by limestone scrub or bare rocks. Fieldworks were carried out by the VRTC in the central part of Cat Ba Island from 10 to 25 October, 2011. In total, 650 trap-nights were conducted using pitfall traps (plastic glasses of 13×9 cm) located in five different biotopes.
Map of Vietnam. Location of islands studied is shown.
A total of thirteen Crocidura specimens were collected during the three aforementioned island surveys. Specimens were fixed in 70% ethanol. Tissue samples were preserved in 96% ethanol. Skulls were extracted and cleaned from many specimens. Standard external body measurements (head and body length, tail length, hind foot length) were taken in the field. Weight was measured in grams. Voucher specimens are kept in the Zoological Institute of the Russian Academy of Sciences (Saint-Petersburg, Russia).
Genomic DNA was isolated from ethanol-fixed kidney or muscles by proteinase K digestion, phenol-chloroform deproteinization and isopropanol precipitation (
The complete mitochondrial cytochrome b gene (cytb, 1140 bp) was amplified by PCR with the primer combination and conditions for cytb amplification as in
GenBank accession numbers for the original sequences used in the study are JX181934-JX181941.
We also included cytb sequence data from several earlier studies (
We have found this species on Con Son Island only. A single specimen was collected near Nui Nha Ban on the north slope of Nui Chua Mt. in the central part of island. The pitfall traps (08°42'49"N, 106°37'13"E) were set in moist primary forest at an elevation of 250 m asl. Despite considerable trapping efforts (more than 1200 trap-nights) we collected only one specimen. This species was firstly reported from Con Son by
This is a large, long-tailed Crocidura; tail 79% of head and body length, on average. Means and extremes of measurements (in mm) from 3 adults are: head and body length, 87.0 (83–90); tail length, 68.3 (67–71); hind foot length, 15.7 (15–17); weight (n=1), 16.7 g.
The mtDNA analysis suggests that specimen from the Con Son Island belongs to Crocidura fuliginosa (Fig. 2).
Many papers listed Crocidura fuliginosa as being widespread in mainland Vietnam (Heaney and Timm 1983;
The occurrence of Crocidura fuliginosa sensu stricto in mainland Vietnam is still questionable (see also
Five adult white-toothed shrews were collected in the northern part of Phu Quoc Island (10°22'53"N, 104°00'19"E), 5 km west of Bai Thom Village, near the road Duong Dong-Bai Thom, close to the northern slope of Mount Chua area, at the elevation of about 30 m asl. Pitfall traps were set up in the dipterocarp forest, near tumbled down trees, at the bottom of a mountain. On the basis on these specimens, Crocidura phuquocensis was described by
This is a medium-sized Crocidura, with a moderately long tail; tail 75% of head and body length, on average. Means and extremes of measurements (in mm) from 5 adults are: head and body length, 76.2 (68–72); tail length, 52.4 (49–59); hind foot length, 12.1 (12–12.5).
The validity of this species was recently confirmed by comparison of cytb and COI sequences with available reference data (
Phu Quoc lies very close to mainland Cambodia. The Phu Quoc rainforests belong to the Cardamom Mountain rain forests ecoregion (
We collected seven specimens of this species from Cat Ba Island. The trapping line (20°48'N, 106°59'E) was located along the west part of tourist trail from the Cat Ba National Park Headquarters to Viet Hai Village. All specimens were caught in pitfall traps set in mixed forest near limestone bare rocks. It is the first record of Crocidura from Cat Ba Island.
This is a medium-sized Crocidura, with a moderately long tail; tail 79.8% of head and body length, in average. Means and extremes of measurements (in mm) from 5 adults are: head and body length, 74.6 (71–79); tail length, 59.2 (57–62); hind foot length, 13.2 (12–14); weight (n=4), 9.8 (7.3–11.5) g.
Analysis of mitochondrial DNA confirmed that the specimens from Cat Ba belong to Crocidura attenuata proper. All the analyzed specimens from Cat Ba (see Fig. 2) formed a single cluster closely related to the group of specimens from northern Vietnam (Ha Giang Province) and southeastern China (Guangxi Province). The genetic distance (p-distance) between specimens from Cat Ba/Ha Giang as well as Cat Ba/Guangxi is about 2.1%. The specimen of Crocidura attenuata from the more north-eastern region of China (Hunan Province) appears basal among all samples of Crocidura attenuata from China and Vietnam. Thus, the genetic distance between two specimens from China (Hunan/Guangxi) is 4.3%, which is nearly the same as the distance between Crocidura indochinensis/Crocidura sp. AB1. Thus, genetic differentiation of Crocidura attenuata is notable and reveals a phylogeographic structure with four haplogroups.
Most authors (
Documentation of Crocidura attenuata on Cat Ba Island well corresponds to the proposed species’ distribution confined to the north and east of the Red River (see
The NJ tree for the cytb gene. The bootstrap values (³50%) obtained from 1000 replications in NJ/MP analyses are presented above the branches. «*» denotes bootstrap support of 100% in both NJ and MP analyses; «-» indicates support values of less than 50%. Suncus murinus and Suncus stoliczkanus are used as outgroup.
Current distributions and phylogenetic relationships of Crocidura species from Vietnamese offshore islands support the hypothesis that shrews may have colonized the islands relatively recently. It is known that the non-volant mammal fauna of these islands was formed during the period when most parts of the modern South China Sea shelf were continental (see also
Cat Ba Island is a part of the extended region of the Viet Bac Karst zone, stretching from southeastern China to northeastern Vietnam (
Sister relationships between the Con Son and Malaysian populations of Crocidura fuliginosa suggest that its distribution might have been more extensive in the past. However, data on this species’ occurrence in Southeast Asia are very scarce and doubtful. Morphological characters and genetic variation of the populations from Thailand, Laos, Cambodia and Myanmar referred to as Crocidura fuliginosa (
We thank the administration of the Joint Vietnam-Russian Tropical Research and Technological Centre, and notably Dr. A.N. Kuznetsov for talented organization of field work. We are grateful to the administrations of the Phu Quoc, Con Dao, and Cat Ba National Parks for providing us with an opportunity to carry out field surveys. AA thanks Dr. A.A. Kalinin and A.V. Shchinov who helped out with field collecting. We are obliged to Dr. D.V. Logunov (Manchester, UK) for linguistic help. We are very grateful to Dr. Manuel Ruedi and two anonymous reviewers for their helpful and constructive comments on the early version of the manuscript. This work was supported in part by the Ministry of Education and Science of Russian Federation and by the Russian Foundation for Basic Research (projects 11-04-00020, 12-04-93005).