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DOES SEXUAL DIMORPHISM EXIST IN SQUIRRELS? A CASE OF FIVE SPECIES
OF GENUS CALLOSCIURUS (CALLOSCIURINAE) OF PENINSULAR THAILAND
WITH KEYS TO SPECIES
Ngagyel Tenzin, 1* Chutamus Satasook, 1, 2 Sara Bumrungsri 1 & Paul J. J. Bates 3
ABSTRACT
Sexual dimorphism of four species of Genus Callosciurus (Callosciurus prevostii, Callosciurus notatus,
Callosciurus caniceps and Callosciurus erythraeus) in Peninsular Thailand was examined. Callosciurus nigrovittatus was excluded owing to lack of data. A series of Mann Whitney test performed showed no significant difference between the sexes (no sexual dimorphism) in the external measurements, although males are slightly larger than most other species. However, Breadth of rostrum and Height of brain case for Callosciurus erythraeus of the male skull was significantly larger than female. In contrast to others, female Callosciurus prevostii is larger than male, but the sample size was too small to make a meaningful conclusion. Dichotomous keys to species are also constructed based on external and cranial characters.
Key words: Callosciurus, dichotomous keys, sexual dimorphism, squirrel.
1Department of Biology, Faculty of Science, Prince of Songkla University, Hatyai 90112, Thailand E- mail : [email protected]
2Princess Maha Chakri Sirindhorn Natural History Museum, Faculty of Science, Prince of Songkla
University, Hatyai 90112, Thailand
3Harrison Institute, Centre for Systematics and Biodiversity Research, Bowerwood House, St. Botolph’s
Road, Sevenoaks, Kent, TN13 3AQ, Great Britian.
u ~ (JPMI INTRODUCTION Sexual dimorphism is a term used to describe any variation between the two sexes within the same species, a pattern shaped due to sexual selection over space and time. Generally both males and females in case of squirrels are same in size and colouration and may be difficult to identify externally (Gorrell et al., 2012). The information on sexual dimorphism is vital for taxonomical and ecological research. For morphometric-based species classification, in the early stage, taxonomists have to examine whether the sexual variation is present in species or not. In terms of ecology, sexual dimorphism can indicate that the food habits of male and female squirrels are different at least during certain times of the year (Koprowski & Corse 2001). This tells us about the intensity of squirrels as pests in different sexes. Understanding this kind of feeding ecology could greatly enhance the understanding of wildlife conservationists and agriculturalists. It would also help understand the nature of dispersal and their significance to ecosystem. For example natal dispersal is believed to be common in birds and mammals, but the pattern is different for males and females (Holekamp & Sherman 1989). It means that the seed dispersed or the pollen carried by these animals is different for males and females. In addition, it is also useful in field of paleontogy and zoonoses. Thus, as a primary gateway to any kind of researches in squirrels, identifying dimorphism is inevitable. Of the large diversity in Southeast Asia, 17 species in 8 genera occur in Thailand which accounts for slightly more than 60 % of the SE Asian squirrels (Lekagul & McNeely 1988; Corbet & Hill 1992; Wilson & Reeder 2005; Francis 2008; Thorington et al. 2012). However, the natural history of most species is poorly known as some of the squirrels are highly variable or taxonomically complex (example: Callosciurus finlaysonii, C. erythraeus and species of genus Tamiops). Koprowski (2008) remarked about the very few scientific publications of squirrels from this region, inspite of the fact that SE Asia is u ~ (JPMI 2008), but with rapid economical development, and population growth, lowland tropical rain forests defragmentation has triggered the significant loss of these rich biodiversity (Tex, 2011). Thus, it has now become a subject of conservation concern and increased effort should be made towards understanding their occurrence, biology and taxonomy in particular. MATERIALS AND METHODS Study site: All of the specimens examined were the voucher specimen from Thailand’s Natural History Museum (THNHM), Pathumthani. A total of 53 skulls and skins [35 ♂♂, 18 ♀♀] were evaluated from 2010 to 2012. To provide insight into further study of these squirrels, localities and list of specimens are provided in the appendix. The geographic coordinates are centered on the locality, when original description was not clear. u ~ (JPMI Figure 1: Distribution map of Specimens of four species of genus Callosciurus in Thailand. Block squares [1-5] = Localities of specimens of Callosciurus prevostii. Open circles [6-15) = Localities of specimens of Callosciurus notatus. Open squares [16-31] = Localities of specimens of Callosciurus caniceps. Block circles [32-53] = Localities of specimens of Callosciurus erythraeus. Refer appendix for details. u ~ (JPMI DATA COLLECTION Measurements: The external measurements and the localities mentioned in the voucher specimens were carefully noted. Skull characters mentioned below were measured up to maximum of 20 adult specimens for one species including males and females (When available). External measurements followed Francis (2008), and cranial measurements followed Lunde & Son (2001). All the measurements were taken using digital caliper. External characters included are: Head and body length (HB): tip of nose to dorsal inflection point of tail, Tail length (T): dorsal inflection point of tail to tip of the last vertebra, Ear length (E): inside of ear from lower notch to outermost margin of pinna, Hind foot length (HF): heel to tip of foot (Excluding claws), Weight (Wt.): body weight. Cranial characters included are: Occipitonasal Length (ONL): The distance from the tip of the nasal to the posterior margin of the occipital, Zygomatic Breadth (ZB): The greatest breadth across the zygomatic arches, Interorbital Breadth (IB): The least distance, as viewed dorsally, across the frontal bones between the orbital fossae, Length of Rostrum (LR): The distance from the tip of the nasal bones to the posterior margin of the zygomatic notch (the anterior edge of the dorsal maxillary root of the zygomatic plate), Height of Braincase (HBC): The distance from the top of the braincase to the ventral surface of the basisphenoid bone, Length of Nasals (LN): The distance from the anterior tip of the nasal bones to the most posterior suture between the nasal and frontal bones, measured parallel to the surface of the nasals, Length of Diastema (LD): The distance from the posterior alveolar margins of the upper incisor to the anterior to the anterior alveolar margins of the first upper molars, Post Palatal Length (PPL): The distance from the posterior margins of the palatal bridge to the posterior edge of the basioccipital bone (the ventral lip of the foramen magnum), Palatal Length (PL): The distance from the anterior u ~ (JPMI (ML): The greatest distance from the most posterior part of the condyle to the most anterior part of the mandible, excluding the lower incisors. Photography: Photographs of voucher specimens of 5 species of the genus were taken to record pelage colour. Photos of skulls were also taken. Data analysis: To determine whether there was sexual dimorphism within the taxa and the significant differences in metric characters (external characters and cranial characters) between taxa, a series of Mann Whitney-test were run at a confidence level of 95%. In addition skull characters were evaluated comparatively to score the diagnostic characters. Principal Component Analysis (PCA) performed on correlation matrix was used for multivariate comparisons for both males and females. RESULT External measurements suggested that females of species Callosciurus caniceps, Callosciurus erythraeus and Callosciurus notatus are slightly smaller than males (Table 1). Similarly 10 cranial characters measured also showed that males are slightly larger than females. However, statistical tests inferred that there is no significant variation between sexes for any of the external measurement. Of 10 cranial characters measured, two were found significant in one species C. erythraeus (Table 2). Breadth of rostrum (BR) and Height of brain Case (HBC) were found significant in Callosciurus erythraeus (Table 2), suggesting BR and HBC in males were larger than females. Also a multivariate analysis (PCA) performed based on 23 cranial characters for both males and females in this species formed discrete grouping indicating sexual dimorphism (Fig. 2). Both external and cranial measurements suggested that females in Callosciurus prevostii have larger skulls, but the sample size (n = 2 ♂♂, n = 2 ♀♀) is too small to make any u ~ (JPMI Figure 2: PCA between the first and the second principal components based on 23 cranial characters for both male and female specimens of genus Callosciurus. CEM = ♂ C. erythraeus, CEF=♀ C. erythraeus, CPM=♂ C. prevostii, CPF=♀C. prevostii, CNM=♂ C. notatus, CNF=♂ C. notatus, CCM=♂ C. caniceps, CCF = ♀ C. caniceps. u ~ (JPMI Table 1: External measurements (Mean, Standard deviation, Minimum & maximum in mm) of four species of Genus Callosciurus. HB = Head body length; T = Tail length; E = Ear length; HF = Hind foot length (claws excluded); Wt (g) = Mean weight in grams; Parenthesis [ ] = sample size; Sex. dim = Sexual dimorphism; ns = not significant; * = Thorington et al. (2012). Species n Sex HB T E HF Wt (g) C. caniceps 12 ♂♂ 241.25, 16.2, 195-240 231.9, 34.4, 172-300 20.5, 1.9, 18-25 48.7, 4.6, 40-56 325[3] 11 ♀♀ 222.3, 16.8, 203-254 225.3, 25.3, 185-260 19.7, 3.8, 11.8-25 47.6, 5.8, 35-54 301.6[3] Sex. dim ns ns ns ns C. erythraeus 14 ♂♂ 226, 22.7, 190-295 181, 26.5, 105-205 19.9, 1.7, 15-22 47.1, 3.6,40-52 345.5[8] 4 ♀♀ 209.2, 8.2, 200-218 181, 35, 130-210 19.2, 4.3, 15-25 49.2, 4.7, 45-56 296.4[1] Sex. dim. ns ns ns ns C. notatus 4 ♂♂ 180, 17.7, 165-200 164.5, 3.3, 160-167 17.2, 1.8, 16-20 46.7, 2.8, 33-40 233.9* 2 ♀♀ 177.5, 31.8, 155-200 185, 35, 160-210 16, 5.6, 12-20 39, 5.6, 35-43 227.9* C. prevostii 2 ♂♂ 277.5, 67.1, 230-325 265, 7, 260-270 25, 0, 25 52.5, 3.5, 50-55 353.7* 2 ♀♀ 262.5, 24.7, 245-280 262.5, 24, 245-280 19.5, 0.7, 19-20 55, 0, 55 237.7* u ~ (JPMI Table 2: Cranial measurements (Mean & Standard deviation (mm)) of four species of genus Callosciurus Species n Sex ONL ZB IB BR HBC LN LD PPL PL ML 54.6, 2.3 31.6, 2.1 19.1, 1.6 14.6, 1.5 18.4, 0.8 17.3, 1.1 13.3, 1 20, 1.3 23.5, 1.2 30.9, 2.2 C.caniceps 12 ♂♂ 11 ♀♀ 54.6, 2.4 30.4, 2.2 18.8, 1.7 14.6, 1.3 18.4, 0.7 16.9, 0. 6 12.5, 1.3 20.3, 1.5 22.9, 1.4 32, 1.2 Sex. dim ns ns ns ns ns ns ns ns Ns ns C. 8 ♂♂ 52.2, 2.1 31.4, 1.4 19.2, 1.1 13.5, 0.7 18.9, 0.7 16.4, 1.1 12.2, 0.7 19.9, 0.8 21.8, 1 30.2, 2.5 erythraeus 3 ♀♀ 51, 0.9 30.6, 1.1 17.8, 0.4 12.4, 0.3 18, 0.2 15.4, 1.1 11.2, 0.2 19, 0.7 21.1, 0.2 30.6, 0.5 ns ns ns Z= -2.04 Z= 2.04 ns ns ns Ns ns Sex dim. p = 0.04 p= 0.04 47.2, 1.6 26.9, 1.2 17.9, 0.7 14, 1.5 18.8, 1.1 13, 0.6 11.2, 0.8 17.9, 0.2 20.1, 0.9 26, 1.4 C. notatus 4 ♂♂ 2 ♀♀ 45.1, 5 25.3, 4.6 15.8, 2.6 12.3, 0.1 17.7, 0.8 12.8, 1.6 10.4, 2.1 16.7, 1.2 19.4, 2.2 27.9, 4.5 2 ♂♂ 56.4, 1.4 33.3, 0.9 22.8, 0.9 18.6, 0.8 17.8, 0.3 19, 0.7 14.6, 0.8 21.9, 0.9 24.6, 1 34.5, 3.3 C. prevostii 2 ♀♀ 60.4, 0.6 36.7, 0.2 25.8, 1.7 17.4, 0.2 20.2, 3.9 21.4, 0.8 15.5, 0.2 23.8, 0.3 22.8, 4.2 36.7, 0.9 u ~ (JPMI SYNOPSIS OF THE DIAGNOSTIC CHARACTERS Numerous researchers used various diagnostic characters. Francis (2008) illustrated the field guide primariily based on dorsal pelage. Thus, whatever descriptions of the pelage colour followed here is based on his excellent work. For better understanding, wherever necessary, illlustrations are provided. Group 1: Head body greater than 270mm and skull length over 55mm: Callosciurus prevostii: This squirrel is the largest among the genera. Its external measurements are significant enough to differentiate (or: to be differentiated from other species) it from other species. It has white stripe that separates the dorsal black pelage and ventor red pelage (Fig 3). A D B C Figure 3: A B & C = Skins of Callosciurus prevostii (THNHM-1963, adult ♀). Scale = 200 mm. D = Lateral view of skulls of C. prevostii (THNHM-1963, adult ♀). Scale = 20 mm. Group 2: Head body less than 270mm and skull less than 55mm: (a).Callosciurus erythraeus (b). Callosciurus caniceps (c). Callosciurus notatus (d). Callosciurus u ~ (JPMI nigrovittatus. All these species are smaller than the C. prevostii. They are further classified into the following two groups. Group 2A: Stripes present on the flank: (a). Callosciurus nigrovittatus (b). Callosciurus notatus. Both species have black and white/pale stripes on the flank that separates the upper and lower pelage. They can be identified by the colour of their belly and by the shape of the frontals on the skull. C. nigrovittatus has grey belly with grey tail. Frontal is flatter. C. notatus has reddish belly with brown tail. The frontal in the skull is not flat (Fig 4). A1 B A2 C D Figure 4: A1 = Lateral view of skin of Callosciurus notatus (THNHM-1935, adult ♀) showing the lateral stripes on the flank. A2 = Ventral view of same skin showing the reddish venter. Scale = 200 mm. B = Lateral view of the maxilla of C. notatus (THNHM-1940, adult ♂) showing the normal frontals. Scale = 20 mm. C = Callosciurus nigrovittatus showing the lateral stripes and greyish beelly/venter. Photo courtesy (Baker 2012, www.arkive.org/black-striped-squirrel/callosciurus- nigrovittatus14/9/2012). D = Skull of C. nigrovittatus showing flatter braincase. Photo courtesy (Lekagul & McNeely 1988). Not to scale. u ~ (JPMI Group 2B: Stripes absent from the flank: (a). Callosciurus caniceps (b). Callosciurus erythraeus Callosciurus caniceps has grey belly but it differs from C. nigrovittatus as it does not have lateral stripes. On the skull there are two pairs of palatine foramen. Callosciurus erythraeus- All the subspecies of the species possess reddish venter in common, but it lacks any stripes, which makes it different from C. notatus. On the skull there are three pairs of palatine foramen. A1 B A2 C1 D C2 Figure 5: A1 = Lateral view of skin of Callosciurus erythraeus (THNHM-1186, adult ♂) showing the absence of lateral stripes. A2 = Ventral view of same skin showing the reddish venter/belly. Scale = 200 mm. B = Lateral view of maxilla of C. erythraeus (THNHM-1156, adult ♂) showing higher height of the braincase. Scale = 20 mm. C1 = Lateral view of skin of Callosciurus caniceps (THNHM-1336, adult ♂) showing the absence of lateral stripes. C2 = Ventral view of same skin showing the u ~ (JPMI grey venter/belly. Scale =200 mm. D = Lateral view of maxilla of C. caniceps (THNHM-1356, adult ♀) showing lower height of braincase. Scale = 20 mm. DICHOTOMOUS KEYS TO SPECIES: 1. HB > 270mm. ONL > 55mm.………….……………………….…………..Callosciurus prevostii. 1' HB < 270mm. ONL < 55mm……………………………..……………………..……………....[2]. 2. Stripes present on the flank……………………………………………….……………………..[2]. 2' Stripes absent from the flank...…………………………………………….………………….....[4]. 3. Grey belly and tip of the tail grey. Frontals flatter…..………………...Callosciurus nigrovittatus. 3' Red belly and tail brown. Normal frontals………………………………....Callosciurus notatus. 4. Grey bellied squirrels. 2 pairs of palatine foramen present……………..…Callosciurus caniceps. 4' Red bellied squirrels. 3 pairs of palatine foramen present……………...... Callosciurus erythraeus. DISCUSSION The statistical test showed that there is a significant difference between the sexes in the species of Callosciurus erythraeus in two cranial characters. These results were u ~ (JPMI based on specimens collected above the Isthmus of Kra as sample size below the Isthmus of Kra was too small (n = 8 ♂♂, n = ♀). However, the males of north of Isthmus of Kra (n = 8) were significantly smaller in four skull characters statistically evaluated (Zygomatic breadth [p-value = 0.015], Inter-orbital breadth [p-value = 0.0.49], Breadth of rostrum [p-value = 0.004] & Height of brain case [p-value = 0.001]) than south of isthmus of Kra (n = 8), which in turn fitted well with the Bergmann’s rule*. But we could not make a meaningful conclusion about sexual dimorphism in case of C. prevostii, C. notatus & C. caniceps. However we doubt that larger sample size may yield significant sexual dimorphism from the cranial measurements. Thus, further study on sexual dimorphism with larger sample size could be carried out in these species. Generally, the average measurements from external and skulls in most species suggested, males are larger except Callosciurus prevostii, in which females seem to be larger (Table 1 & 2). Males in this species were smaller externally. Also 23 cranial characters measured and tested showed the similar pattern. In addition, while constructing keys to five species of Callosciurus based on our data, we followed McNeely & Lekagul (1988) wherever necessary, but the groupings were changed as their dichotomous keys considered some species of genus Sundsciurus as one genus Callosciurus. Also they considered Callosciurus flavinmanus as an independent species, which is treated subspecies of Callosciurus erythraeus currently (Wilson & Reeder, 2005; Francis, 2008; Thorington et al., 2012). However, it is important to note that the sexual dimorphism tested here does not apply to all the 17 species of Non-flying squirrels recorded in Thailand. u ~ (JPMI CONCLUSION Morphometric analysis for five external measurements and 23 cranial measurements were considered for statistical testing for sexual dimorphism. In addition morphology of the skins and skulls were evaluated and the dichotomous keys were constructed to help in identifying the species in this genus. ACKNOWLEDGEMENT We are most grateful to the Director of Thailand Natural History Mueseum (THNHM), Dr. Somchai Bussarawit and Director of Reference Collection Division Mr. Tanya Chan-ard for their kind hospitability and help for this study. Special thanks are due to staffs of THNHM; Mr. Yutthapong Rassameee and Mr. Anupas Rattanathavorn for helping to take excellent pictures; Mr. Cholawit Thongcharoenchaikit and Mr. Sunchai Makchai for being a brilliant translator during the study in the museum; Dr. Yodchai Chuaynkern for providing accommodation. Thanks are due to Dr. Prateep Duengkae at Forest Biology Department, Faculty of Forestry, Kasetsart University, for providing an opportunity to present the research in Thailand Wild life Seminar. Thanks are also due to the students of Birds and mammals research unit at Prince of Songkla University, Faculty of Science. Finally we would like to thank the graduate school of Prince of Songkla University and the British government for their financial support for this project through Darwin Initiative, and Faculty of Science, Prince of Songkla University for providing scholarship to Mr. Ngagyel Tenzin. 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The Johns Hopkins University Press, Maryland. u ~ (JPMI APPENDIX 1 List of specimens Callosciurus prevostii - [Skins] THNHM-1953-53, 62-63, 3♂♂ + 2♀♀, [Skull] THNHM- 1953-54, 62-63 2♂♂ + 2♀♀, Krabi Province (Ban Khuan Daeng, Khlong Thom District, 8° 0.780'N, 99° 14.340'E, 82 m), Trang Province (Muang, Khao Chong, Na Yong District, 7° 33.427'N, 7° 33.427'E, 423 m), Phatthalung Province (Khao Chong, Khao Phub Pa, 7° 34.971'N, 99° 59.473'E, 31 m); Callosciurus notatus - [Skins] THNHM-1935-36, 38, 40,48-50, 52, 4♂♂ + 4♀♀, [Skulls] THNHM-1940, 48-49, 50,52, 3♂♂ + 2♀♀, Krabi Province (Ban Khuan Daeng, Khlong Thom District, 8° 0.780'N, 99° 14.340'E, 82 m), Nakhon Si Thammarat Province (Khok Chang Bang, Thung Yai District, 8° 25.745'N, 99° 31.793'E, 47 m; Namtok Ta-Pae, Chawang District, 8° 25.745'N, 99° 31.793'E, 47 m), Narathiwat Province (Ba Joh water fall, Joh Hai Rong District, 6° 11.406'N, 101° 47.878'E, 541 m), Ranong Province (Ban Bang Bane, Kapur District, 10° 0.966'N, 98° 42.560'E, 122 m); Callosciurus caniceps - [Skins=Skulls] THNHM-1306,08,13,21,27,47,48,52- 53,56,58,60,80, 86, 9, THNHM-1299, 9♂♂ + 6♀♀, Chiang Mai Province (Ban Tham, Chiang Dao District, 19° 23.676'N, 98° 55.740'E, 438 m), Kanchanaburi Province (Thong Pha Poom, Thong Pha Poom District, 14° 3.519'N, 99° 27.977'E, 40 m), Nakorn Ratchasima Province (Sakaerat, Pak Thong Chai District, 14° 43.183'N, 102° 1.283'E, 208 m), Nan Province (Sa, Ban Pha Hang, Phu Pheang District, 18° 41.089'N, 100° 48.000'E, 250 m), Pattani Province (Nam Tok Sai Khao, Na-Pradu District, 6° 51.983'N, 101° 22.150'E, 6 m), Phang-nga Province (Koh Yao Yai, Koh Yao District, 8° 2.809'N, 98° 34.983'E, 185 m), Ranong Province (Huang, Ban Bang Non, 10° 0.966'N, 98° 42.560'E, 122 m; Koh Surin Nua, Kapoe, 10° 0.966'N, 98° u ~ (JPMI 42.560'E, 122 m), Saraburi Province (Kaeng Khoi, Phu Nam Tok Tap Kwang, 14° 29.863'N, 100° 53.419'E, 12 m), Satun Province ( Koh Ta Ru Tao, 6° 32.971'N, 99° 40.147'E, 37 m), Surat Thani Province (Muang, Khao Tha-Pet, 8° 54.204'N, 99° 0.774'E, 118 m) , Uthai Thani Province (Kaen-Ma-Krud; E-Sai, Ban Rai District, 14° 3.519'N, 99° 27.977'E, 40 m); Callosciurus erythreaus - [Skins] THNHM-1153- 57, 84-88, 95-98, THNHM-1204, 06-07, 14, 17-18,28, 17♂♂ + 4♀♀, [Skulls] THNHM-1153-56, 84-88, 96-98, THNHM-1204, 06-07, 14, 17-18, 28,16♂♂ + 3♀♀, Chiang Mai Province (Ban Tham, Chiang Dao District, 19° 23.676'N, 98° 55.740'E, 438 m; Chom Thong, Doi Inthanon, Mae Jam District, 18° 34.791’N, 98° 28.996’E, 2475 m; Hot, Ban Bo Luang, Mae Jam District, 18° 24.480'N 98° 25.565'E, 745 m; Mae Taeng, Doi Pui, 18° 49.996'N, 98° 54.001'E, 1290 m), Kanchanaburi Province (Mae Nam Noi, Sai Yok District, 14° 25.261'N, 98° 50.701'E, 80 m), Mae Hong Son Province (Huai Ko Mong, Mae Saring District, 18° 10.278'N, 97° 55.940'E, 228 m), Nakhon Pathom Province (Phrong Madua; 64km from Bangkok, 13° 58.733'N, 100° 10.220'E, 4 m), Nakhon Si Thammarat Province (Khao Luang, Phrom Khiri District, 8° 29.654'N, 99° 43.802'E, 1756 m), Uthai Thani Province (Kaen-Ma-Krud; E-Mard, Ban Rai District, 15° 5.033'N, 99° 31.267'E, 160 m. u ~ (JPMI APPENDIX 2 List of localities in Figure 1 Localiies [1-5] = Callsocirus prevostii, Localities [6-15] = Callosciurus notatus, Localities [16-31] = Callosciurus caniceps, Localities [32-53] = Callosciurus erythraeus. Locality [1]: Ban Khuan Daeng, (Khlong Thom, District), Krabi Province, Thailand (8° 0.780'N, 99° 14.340'E, 82 m), Locality [2-4]: Khao Chong, Phatthalung Province, Thailand (7° 34.971'N, 99° 59.473'E, 31 m), Locality [5]: Khao Chong, (Na Yong District), Trang Province: Thailand (7° 33.427'N, 7° 33.427'E, 423 m), Locality [6-7]: Ban Khuan Daeng, (Khlong Thom District), Krabi Province, Thailand (8° 0.780'N, 99° 14.340'E, 82 m), Locality [8-10]: Ban Ta Pae, (Chawang District), Nakorn Si Thammarat, Thailand (8° 25.745'N, 99° 31.793'E, 47 m), Locality [11]: Ba Joh waterfalls, (Joh Hai Rong District), 31km NE of Narathiwat, Thailand (6° 11.406'N, 101° 47.878'E, 541 m), Locality [12-15]: Ban Bang Bane, (Kapur District), Ranong Province, Thailand (10° 0.966'N, 98° 42.560'E, 122 m), Locality [16]: Ban Tham, (Chiang Dao District), Chiang Mai Province, Thailand (19° 23.676'N, 98° 55.740'E, 438 m), Locality [17-19]: Huai Kha Yaeng, (Thong Pa Phoom District), Kanchanaburi Province, Thailand (14° 3.519'N, 99° 27.977'E, 40 m), Locality [20]: Sakaerat, (Pak Thong Chai District), Nakhon Ratchasima Province, Thailand (14° 43.183'N, 102° 1.283'E, 208 m), Locality [21]: Sa Ban Pha Hang, (Phu Phiang District), Nan Province, Thailand (18° 41.089'N, 100° 48.000'E, 250 m), Locality [22]: Nam Tok Rai Kao, (Na-Pradu District), Pattani Province, Thailand (6° 51.983'N, 101° 22.150'E, 6 m), Locality [23-24]: Koh Yao Yai, (Koh Yao District), Phang-nga Province, Thailand (8° 2.809'N, 98° 34.983'E, 185 m), Locality [25]: Koh Surin Nua, u ~ (JPMI Kapoe, Ranong Province Thailand (10° 0.966'N, 98° 42.560'E, 122 m), Locality [26- 27]: Huang, Ban Bang Non, Ranong Province, Thailand (10° 0.966'N, 98° 42.560'E, 122 m), Locality [28]: Kaeng Khoi, Phu Nam Tok Tap, (Khwaeng District), Sara Buri Province, Thailand (14° 29.863'N, 100° 53.419'E, 12 m), Locality [29]: Koh Ta Ru Tao, Satun Province, Thailand (6° 32.971'N, 99° 40.147'E, 37 m), Locality [30]: Khao Tha-pet, (Muang District), Surat Thani Province, Thailand (8° 54.204'N, 99° 0.774'E, 118 m), Locality [31]: Kaen-Ma-Krud E-Sai, (Ban Rai District), Uthai Thani Province, Thailand (14° 3.519'N, 99° 27.977'E, 40 m), Locality [32]: Hot, Ban Bo Luang, (Mae Jam District), Chiang Mai Province, Thailand (18° 24.480'N 98° 25.565'E, 745 m), Locality [33]: Doi Puik, Chiang Mai Province, Thailand (18° 49.996'N, 98° 54.001'E, 1290 m), Locality [34]: Ban Tham, (Chiang Dao District), Chiang Mai Province, Thailand (19° 23.676'N, 98° 55.740'E, 438 m), Locality [35]: Chom Thong Doi Inthanon, (Mae Jam District), Chiang Mai Thailand (18° 34.791'N, 98° 28.996’E, 2475 m), Locality [36]: Mae Nam Noi, (Sai Yok District), Kanchanaburi Province, Thailand (14° 25.261'N, 98° 50.701'E, 80 m), Locality [37- 38]: Huai Ko Mong, (Mae Saring District), Mae Hong Son Province, Thailand (18° 10.278'N, 97° 55.940'E, 228 m), Locality [39-40]: Phrong Madua-64km from Bangkok, (Bang Lane District), Nakhon Pathom Province (13° 58.733'N, 100° 10.220'E, 4 m), Locality [41-51]: Khao Luang, (Phrom Khiri District) Nakhon Si Thammarat Province (8° 29.654'N, 99° 43.802'E, 1756 m), Locality [52-53]: Kaen- Ma-Krud, E-Mard, (Ban Rai District), Uthai Thani Province, Thailand (15° 5.033'N, 99° 31.267'E, 160 m). u ~ (JPMI