Murina hkakaboraziensis, Renner, Swen C., 2017

Renner, Swen C., 2017, A new species of Murina (Chiroptera: Vespertilionidae) from sub-Himalayan forests of northern Myanmar, Zootaxa 4320 (1), pp. 159-172 : 161-166

Murina hkakaboraziensis sp. nov.

( Figs. 1–4 ; Table 1 )

Holotype. Adult male, field number PS160218.6, (to be subsequently deposited at the Zoological Collection of the University of Mandalay ( UMZC), Myanmar), body in alcohol, skull and baculum extracted.

Type locality. Myanmar, Kachin, Putao Township, Hkakabo Razi National Park (proposed southern extension), 6 km north of Mali Raing Village, 27°37’19” N, 97°22’13” E, 510 m a.s.l., collected on 18 February 2016, by Pipat Soisook, Sai Sein Lin Oo and Awatsaya Pimsai.

Diagnosis. A small tube-nosed bat with a FA of 29.6 mm. The external appearance is characterised by generally orange-brown pelage on the dorsal and whitish-grey on the ventral side; with long bright golden tip guard hairs on the dorsal side, most densely on the top of the head and the forehead. In the skull, the forehead profile rises smoothly to the braincase, which is relatively high but not dome-shaped. The sagittal crest and lambdoid crest are absent. The upper canine exceeds the posterior upper premolar in height and is slightly more than half of its crown area. The mesostyles on the first and second upper molars are well developed. The talonids of both first and second lower molars are equal to that of their respective trigonids in size.

Etymology. The species is named after the Hkakabo Razi Landscape, where the only known specimen was collected. The proposed English name is ‘Hkakabo Razi Tube-nosed Bat’.

Description. This is a very small vespertilionids with a FA of 29.6 mm and HB of 35.5 mm ( Table 1 ). The pinna is rounded, with 17.0 mm in height, and is without distinct emargination on the posterior border. The tragus is relatively short, shorter than half of the pinna ( Fig. 1a ), with a height of 7.5 mm ( Table 1 ). The body is covered with long hairs, particularly on the head ( Fig. 1a ). The most distinctive feature of the pelage is long bright golden hairs over the back of the head ( Fig. 1a ). The face and forehead are covered with very short dark brown hairs. The pelage on the dorsal side is greyish-brown basally and orange-brown at the tips ( Fig. 1b ); the very long and bright golden guard hairs are sparsely distributed over the back and tail membrane, but are more plentiful on the head ( Fig. 1a ). The pelage on the ventral side is very dark at the base, followed by grey in the middle and with a whitishgrey tip ( Fig. 1c ). The wing membrane is attached to the base of the claw of the outer toe. The foot is relatively large, 8.6 mm, which is more than half of the tibia length ( Table 1 ).

In the skull, the small and shortened first upper premolar (P2) indicates that this species belongs to the suillia - type. The GTL and CCL are 13.82 mm and 12.35 mm, respectively ( Table 2 ). The rostrum is deep and bulbous. The interorbital region is deeply concave when viewed from above. The lateral profile of the forehead rises gradually and smoothly to the braincase ( Fig. 2a ). The braincase is relatively high (BH 6.02 mm) but not domed in shape. The sagittal crest and lambdoid crest are absent ( Fig. 2a ). Each zygoma is thin and without a dorsal process. The upper toothrows converge anteriorly ( Fig. 2a ); C1–C1 is 62.6% of M3–M3. The C–M3 is 4.75 mm ( Table 2 ). The inner upper incisor (I2) is slightly longer than the outer one (I3) and is about half the crown area ( Fig. 2a ). The secondary cusp of the I3 is well developed and is about half the height of the main cusp. The I3 is relatively large, its crown area is about two-thirds that of the upper canine (C1) and subequal to that of the posterior upper premolar (P4) ( Fig. 2a ). The C1 is rounded in shape and without a lingual cusp at its base. It is about two-thirds that of P 4 in crown area. In the lateral view, the C1 slightly exceeds the P 4 in height ( Fig. 2a ). The anterior upper premolar (P2) is small, broader than long. It is slightly less than half that of the P 4 in crown area and about half the height ( Fig. 2a ). The labial surface of the first (M1) and second (M2) upper molars is W-shaped ( Fig. 2a ). The mesostyles of both M1 and M2 are well developed.

In the mandible, the toothrow length (C-M3) is 5.15 mm. The lower canine (C1) is relatively small, but exceeds the anterior (P2) and the posterior lower premolar (P4) in both height and crown area ( Fig. 2a ). The cingulum of the C1 is well-defined and possesses a small anterior cusp. The anterior lower premolar (P2) is slightly more than half that of the C1 and about two-third that of the P 4 in height. Its crown area is about half that of the C1 and two-thirds of the P4 ( Fig. 2a ). The P4 is about two-thirds that of the C 1 in both height and crown area. The first and second molars (M1 and M2) are relatively large in comparison with the C1, such that the C1 is only about slightly more than half the crown area of the M1 and M2. The crown area of the talonid of both M1 and M2 is about equal to that of its respective trigonid ( Fig. 2a ). The coronoid process is projected slightly forward and relatively low with a CPH of 2.95 mm ( Table 2 ).

The baculum is very small with a total length of 0.8 mm and 0.6 mm in width ( Fig. 3 ). It is somewhat rectangular in shape and without constriction ( Fig. 3 ). The dorsal side is arch upward.

Echolocation. Currently, for M. hkakaboraziensis sp. nov., echolocation calls are only known from the holotype. Unfortunately, the calls were relatively faint and it was not possible to record a good signal of the initial hook. This made it impossible to measure the start frequency (sf) accurately. Nevertheless, it is possible to describe that this Murina emits broadband frequency modulated (FM) signals typical of the genus with a highest frequency (hf) of 164.0–169.0 kHz. The energy is distributed almost evenly throughout the pulse, with an fmaxe between 148.5 and 152.8 kHz. The terminal frequency (tf) varied from 62.0–70.0 kHz. The call duration (d) was 3.0–3.8 ms and the inter-pulses interval (ipi) was 69.1–75.3 ms. Echolocation characters indicate that this species, as many other Murina , is a forest-adapted species. However, based on the habitat of the capture site (see below), it is likely that it is adaptable to forage around edges between forest and open space.

Genetics. The Bayesian analysis phylogram based on DNA barcode reveals that several species in the subfamily Murininae are paraphyletic ( Fig. 4 ). The single specimen of M. hkakaboraziensis sp. nov. clustered in a distinct but monophyletic clade with M. kontumensis from south-central Vietnam ( Fig. 4 ). However, it has a genetic distance, based on COI, of 11.5% from M. kontumensis . This estimate evolutionary divergence is relatively large for intraspecific variation within Murina species, but it is typical between morphologically similar sister species, e.g. M. chrysochaetes vs M. harpioloides (11.9%; Eger & Lim, 2011). It is interesting to note that based on COI sequences the specimens of M. cf. eleryi from the same locality as the new species, although clustered closely with other specimens of M. eleryi , form a distinct clade and are more similar with M. balaensis from peninsular Thailand (K2P 9.3%) than with specimens from elsewhere in Indo-China (10.5%) ( Fig. 4 ). It is very likely that M. eleryi has a complex biogeographic pattern, as mentioned in Son et al. (2015). Further study may demonstrate that the population of ‘ M. cf. eleryi’ in the Hkakaborazi Landscape has a distinct genetic structure, reflecting its demographic history, e.g. paleo-refuges, and that it is another undescribed cryptic species (P. Soisook, unpublished data).

Comparison with similar species. Murina hkakaboraziensis sp. nov. differs from Murina species in the cyclotis- type in having relatively small P2. Among species with a suilla- type morphology, it can be separated from most species by a combination of its relatively small size (FA 29.6 mm; GTL 13.82 mm – Table 1 and 2 ), and pelage colour, having grey hairs on the belly and orange-brown hairs on the back with long golden guard hairs on the head and back. It is relatively similar in body size to M. harpioloides and M. chrysochaetes ; it also shares the character of having golden hairs. However, it differs genetically and in other details of the pelage colouration and craniodental morphology. Murina harpioloides has a more orange colouration and the sagittal and lambdoid crests, although very weak, are present ( Kruskop & Eger 2008; Son et al. 2015); they are absent in M. hkakaboraziensis sp. nov. In M. chrysochaetes , the ventral pelage has golden hairs as on the dorsal side ( Eger & Lim 2011), but in M. hkakaboraziensis sp. nov., the golden hairs are only apparent on the dorsal side ( Fig. 1 ). The slope of the forehead of M. chrysochaetes is abrupt and the braincase is high and dome-shaped ( Eger & Lim 2011), but the forehead profile of the new species gradually slopes up to the braincase, which although relatively high, is not dome-shaped ( Fig. 2a ). The pelage appearance of the new species is also somewhat similar to Harpiola isodon and M. lorelieae , but both of them have a larger body size and differ in the shape of the cranium ( Kuo et al. 2006; Eger & Lim 2011; Son et al. 2015).

Murina hkakaboraziensis sp. nov. is most similar to the Vietnamese M. kontumensis , which was very recently described from south-central highland of Vietnam ( Son et al. 2015). However, M. hkakaboraziensis sp. nov. has a more plentiful and well-defined longer bright golden guard hair ( Fig. 1a ). Besides the bright golden guard hairs, the colouration of the pelage on the dorsal and ventral sides are also different. In M. kontumensis , the general impression of the hairs are brownish-grey on the dorsal side and light brown on the ventral side, whereas M. hkakaboraziensis sp. nov., is orange-brown on the dorsal side ( Fig. 1b ) and whitish-grey on the ventral side ( Fig. 1c ). There is no contrasting whitish collar around the neck of M. hkakaboraziensis sp. nov. ( Fig. 1a ), but this whitish collar is very obvious in M. kontumensis ( Son et al. 2015, figure 3A). The wing membrane of the new species is attached about 2 mm above the base of the claw of the outer toe, whereas it attached to the base of the claw in M. kontumensis ( Son et al. 2015, figure 3H). In the cranium, the lateral profile of the interorbital region of M. kontumensis rises abruptly to the forehead, but rises smoothly and gradually in M. hkakaboraziensis sp. nov. ( Fig. 2 ). The sagittal crest of M. kontumensis is well-defined but it is absent in the new species ( Fig. 2 ). In the dentition, the secondary cusp of the I3 of M. hkakaboraziensis sp. nov. is very well developed and is about half the height of the main cusp, but in M. kontumensis this cusp is very poorly developed and is less than one-third the height of the main cusp ( Fig. 2b ). The posterior upper premolar (P4) of M. hkakaboraziensis is somewhat square ( Fig. 2a ) and larger in crown area than that of M. kontumensis , which is rectangular, broader than long ( Fig. 2b ). Subsequently, the upper canine (C1) of M. hkakaboraziensis sp. nov. appears to be relatively smaller in crown area than in M. kontumensis when comparing to the P4.

Ecology and distribution. The new species, M. hkakaboraziensis sp. nov., was collected in a mist net set at the edge of a lowland semi-evergreen forest at the transition zone to an open space grassland, which undergoes an annual burn ( Fig. 5 ). The new species was the only bat captured in the mist net. However, on the same night, four other insectivorous bats, Rhinolophus affinis , R. pusillus , Aselliscus stoliczkanus and Hipposideros pomona were captured in nearby mist nets and harp traps. Four other vespertilionids, M. cyclotis , M. feae , M. cf. eleryi , Kerivoula hardwickii , and K. furva were also captured in the same area on other nights. Currently, the new species is only known from the holotype collected from the type locality in the Hkakabo Razi Landscape, Kachin, northern Myanmar.

Figures

FIGURE 1. The appearance of the face, ear and pelage (a), dorsal pelage (b), and ventral pelage (c) of M. hkakaboraziensis sp. nov., ♂ PS 160218.6, holotype, from Kachin, Myanmar.

FIGURE 2. Comparison of the skull of M. hkakaboraziensis sp. nov., ♂ PS 160218.6, holotype, from Kachin, Myanmar (a), and M. kontumensis ♀ IEBR-M 5697, holotype, from Kon Tum, Vietnam (b).

FIGURE 3. The dorsal side of the baculum of M. hkakaboraziensis sp. nov., ♂ PS 160218.6, holotype, from Kachin, Myanmar. Scale = 1 mm. Drawing by PS.

FIGURE 4. Bayesian tree based on GTR + I + G of 157 COI sequences of bats in the subfamily Murininae with a Kerivoula cf. hardwickii as an outgroup. The posterior probabilities of branch support are shown on branches.

FIGURE 5. The edge of a lowland semi-evergreen forest at the transition zone to an open space grassland where the specimen of M. hkakaboraziensis sp. nov. was captured. Photograph by SSLO.

Tables

TABLE 1. Mean±standard deviation (SD), minimum-maximum values of mass and external measurements of M. hkakaboraziensis sp. nov. and other comparative Murina species. Total sample size of male and female are given. Sample sizes that differs from stated sample size are in brackets. List of specimens in the Appendix.

Species	n Sex	MASS	FA	E	TRG	HB	TL	TIB	HF
M. hkakaboraziensis	3	3.4	29.6	17.0	7.5	35.5	30.1	15.5	8.6
sp. nov.	(holotype)
M. kontumensis	♀	5.0	32.3	18.7	7.4	40.0	38.5	16.2	7.6
	(holotype)
M. harpioloides	3	-	28.9	11.3	6.0	32.1	20.2	12.1	6.8
	♀	-	28.4	10.1	5.4	34.2	20.7	11.6	6.4
M. eleryi	2 3	-	27.7 [1]	11.8 [1]	5.6 [1]	-	26.5 [1]	13.9 [1]	5.6 [1]
	5♀	5.5 [1]	29.0, 30.4	12.0, 12.4	5.7, 6.1	35.9, 37.8	31.7, 32.6	13.2, 14.8	7.4, 7.5
M. walstoni	2 3	5.2 [1]	28.1, 33.4	11.9, 14.5	6.8, 8.2	34.8, 45.4	31.0, 33.6	15.1, 15.9	6.8, 7.0
	5♀	5.1 [1]	32.8±2.9	13.6±1.5	7.5±0.4	42.6±1.5	33.2±1.1	16.2±0.9	7.6±0.5
			29.4 – 34.7 [3]	12.5 – 14.7 [2]	7.3 – 7.8 [2]	41.6 – 43.6 [2]	32.4 – 33.9 [2]	15.3 – 17.0 [3]	6.9 – 8.0 [3]
M. feae	12 3	4.7±0.3	30.1±0.8	11.9±2.6	6.17 [1]	38.1±2.6	34.3±3.3	17.0±0.3	5.9±1.4
		4.5 – 5.0 [3]	29.0 – 31.5 [9]	8.2 – 14.0 [4]	-	35.0 – 41.4 [4]	31.0 – 39.0 [4]	16.7 – 17.5 [4]	5.1 – 8.0 [4]
	14♀	5.2±0.3	32.0±2.2	12.8±1.5	6.8±0.8	41.2±3.0	35.8±4.4	17.5±1.2	7.1±0.7
		5.0 – 5.4 [2]	28.6 – 36.0 [12]	9.7 – 14.5 [9]	5.7 – 7.5 [5]	39.5 – 48.0 [7]	28.2 – 40.4 [10]	16.0 – 19.5 [11]	5.8 – 7.8 [11]
M. ussuriensis	2♀	-	26.7 [1]	-	-	-	-	-	-

TABLE 2. Mean ± standard de iation (SD), minim m—maxim m al es of craniodental meas rements of M. hkakaboraziensis sp. no. and other comparati e Murina species. Sex and total sample size are i en. Sample sizes that differs from stated sample size are in rac! ets. " ist of specimens in the # ppendix.

Species	n Sex	$%"	S%&%"	CB"	CC"	ZB	PC	BB	MW
M. hkakaboraziensis	3	1³.82	14.0³	1³.05	12.³5	7.74	³.68	6.70	6.98
sp. nov.	(holotype)
M. kontumensis	♀	15.³0	14.90	14.16	1³.7	8.70	4.02	7.³5	7.47
(holotype)
M. harpioloides	3	14.70	14.61	1³.28	12.50	8.44	4.³4	7.46	7.55
	♀	14.³4	14.18	1³.10	12.54	8.29	4.15	7.12	7.28
M. eleryi	2 3	14.15, 14.³7	14.21	12.91±0.10	12.³5±0.25	7.92±0.20	4.15±0.02	6.88±0.14	7.10±0.09
		[2]	[1]	12.84—1³.0³	12.09—12.59	7.69—8.05	4.1³—4.16	6.74—7.02	7.04—7.21
	5 ♀	14.75±0.50	14.12	1³.57 ±0.³6	12.84±0.27	8.19±0.14	4.1³±0.19	6.99±0.05	7.29±0.04
		14.17—15.04	[1]	1³.17 —1³.88	12.54— 1³.05	8.05—8.³2	³.99 —4.³5	6.95—7.05	7.25—7.³³
M. walstoni	2 3	14.48, 15.7³	-	1³.0³, 14.74	12. ³5, 1³.94	7.69, 9.04	7.08, 7.50	7.05, 7.65	4.16, 4.20
	5 ♀	16.1³±0.22	-	14.66±0.19	1³.89 ±0.18	9.1³±0.21	4.21±0.12	7.5³±0.1³	7.8³±0.19
		15.89—16.³7	-	14.4³—14.90 [4]	1³.68 —14.11 [4]	8.9³—9.42 [4]	4.08—4.³7 [4]	7.³7—7.68 [4]	7.68—8.11 [4]
M. feae	12 3	15.³8±0.1³	-	14.00±0.1³	1³.³6±0.15	8.64±0.14	4.³4±007	7.45±0.16	7.³6±0.14
		15.25—15.55 [6]	-	1³.77 —14.14 [6]	1³.10 —1³.54 [6]	8.4³8.75 [6]	4.24—4.40 [6]	7.17—7.62 [7]	7.18—7.55 [5]
	14 ♀	16.07±0.56	-	14.72±0.52	14.01±0.47	8.84±0.³4	4.4³±0.19	7.50±0.³2	7.56±0.18
		14.71—16.74 [1³]	-	1³.66 —15.58 [1³]	12.96—14.78 [1³]	8.³5—9.4³ [12]	4.12—4.86 [1³]	6.77—8.12 [1³]	7.25—7.94 [1³]
M. ussuriensis	2 ♀	14.70, 15.³9	14.17 [1]	1³.11, 14.50	12.³0 [1]	7.75, 8.57	4.09, 4.³5	6.85, 7.27	7.07 [1]
M. beelzebub	1 ♀	16.62	16.³7	15.22	14.59	9.77	4.86	8.28	8.04
	1 ♀	16.74	16.4³	15.7	14.86	9.³6	4.8³	8.14	7.96
M. puta	2 ♀	17.67, 17.9³	17.02, 17.29	16.78, 17.14	16.04, 16.29	9.68, 10.54	4.50, 4.68	7.69, 7.99
M. leucogaster	1 ♀	19.0³	18.78	18.0³	17.22	11.³6	5.18	8.71	9.59

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