Miniopterus phillipsi, Kusuminda & Tharaka & Mannakkara & Amani & Ukuwela & B. & Kruskop & V. & Amarasinghe & J., 2022

Kusuminda, Tharaka, Mannakkara, Amani, Ukuwela, B., Kanishka D., Kruskop, V., Sergei, Amarasinghe & J., Chamara, 2022, DNA Barcoding and Morphological Analyses Reveal a Cryptic Species of Miniopterus from India and Sri Lanka, Acta Chiropterologica 24 (1), pp. 1-17 : 4-10

Miniopterus phillipsi sp. nov. Phillips’s Long fingered Bat

Synonymy

Miniopterus schreibersii Blanford, 1891 (in part): not Vespertilio schreibersii Kuhl, 1817 .

Miniopterus fuliginosus Tian et al., 2004 (in part): not Vespertilio fuliginosus Hodgson, 1835 .

Holotype

NMSL 2021.03.01.NH (field no. TK0122), collected by Tharaka Kusuminda and Mathisha Karunarathne on 29 January 2019. An adult female preserved in 70% alcohol and deposited at National Museum of Sri Lanka, the skull has been extracted and cleaned. There is a scar on left shoulder of the specimen made while collecting the tissue sample. Its partial COI sequence is available from GenBank as accession OL688878 .

Type locality

Idulgashinna cave , near Idulgashinna railway station (6.779131 N, 80.896704 E; 1590 m a.s.l. — Fig. 3 and Supplementary Fig. S2 ), at an edge of Dunkanda division of Bio Tea Garden tea plantation in the Badulla District, Uva Province, Sri Lanka. The holotype was collected in a harp trap set in front of the cave entrance.

Paratypes

Two adult male specimens NMSL 2021.03.02.NH and NMSL 2021.03.03.NH , collected at the same locality as the holotype on 29 January 2019 ( Fig. 4 ). These two specimens are currently preserved in 70% alcohol at National Museum of Sri Lanka. Tongue muscle of NMSL 2021.03.02.NH was preserved in 99% ethanol. The skulls were extracted and cleaned. The paratypes were not sequenced.

Referred specimens

Two specimens ( NMSL 177C and NWRTC TK156 ) were collected from mid-elevations in Kegalle District of Central Sri Lanka (a cave in Sandaraja forest, Doteloya , Aranayaka , Sri Lanka on 02 January 2019 ). These two specimens have not been sequenced for COI gene, but one ( NMSL 177C ) has been sequenced for the mitochondrial 16S gene and was determined to be the same species (T. Kusuminda, A. Mannakkara, K. D. B. Ukuwela, M. Karunarathna, B. D. Patterson, and W. B. Yapa, In litt.). Moreover, these two specimens are morphologically identifiable as M. phillipsi sp. nov. by LDA. A biopsy punch was obtained from a Miniopterus captured and released (field no. TK0064) near the Tea Research Institute in Nuwara Eliya District (Talawakele, Sri Lanka on 02 October 2018). This individual’s COI sequence (GenBank no. OL 688877 ) was 98% similar to the holotype’s sequence, hence it was identified as M. phillipsi sp. nov. Another three specimens ( NMSL 177D, NWRTC TK117 and HZM 263.29194 ) were collected from Wavulgalge cave , Nikapitiya, Wellwaya (Moneragala District of Sri Lanka) and four specimens ( NMSL 177E , HZM 260.27644 , HZM 261.27645 and HZM 262.29137 ) were collected from Wavulpane cave , Pallebedda (Ratnapura District of Sri Lanka) . These seven specimens have not been sequenced but morphological similarities and LDA assignments provisionally assign them to M. phillipsi sp. nov. Likewise, 18 specimens collected from Western India ( HZM 258.25669 , HZM 254.25009 , HNHM 92.156.1 – HNHM 92.124.16 ) have not been sequenced but were identified morphologically as M. phillipsi sp. nov. using LDA ; they were obtained from the same colony where a genotyped individual for COI gene (GenBank no. MG821206 — C. Srinivasulu, B. Srinivasulu, T. A. Shah, and G. Devender, unpublished data) was collected, i.e. Robbers’ Cave, near Mahabaleswar, Maharashtra, India ( Fig. 3 ).

Etymology

This species is named after W. W. A. Phillips (William Watt Addison Phillips, 1892–1981) in recognition of his immense contributions to studies on the mammals of Sri Lanka and South Asia. Phillips was born and grew up in England and he was a nature lover since his childhood. He was a tea planter by profession and came to Ceylon (now Sri Lanka) in 1911.

Diagnosis

Miniopterus phillipsi sp. nov. is distinguished by its intermediate size from both smaller and larger congeners in India and Sri Lanka. M. pusillus is much smaller than M. phillipsi sp. nov. in the external measurements TIB (<18 mm), FA (<43 mm), d 3m (<40 mm), d 4m (<38 mm) and d 5m (<36 mm) and in skull length (GSKL <14.7 mm). M. phillipsi sp. nov. is distinguished from M. magnater by the latter’s larger external measurements (HB> 56 mm and d 3m> 46 mm) and skull size (GLSK> 16.4 mm — Tables 3 and 4). The new species is generally smaller than M. fuliginosus in both external and cranial dimensions, although there is slight overlap ( Figs. 5–7 ). There are significant differences between M. phillipsi sp. nov. and M. fuliginosus in GSKL (P <0.001), ZYW (P = 0.026), MAW (P <0.001), BCW (P = 0.046), LW (P = 0.001), ML (P = 0.001), M3–M3 (P = 0.002), C–M3 (P = 0.002), I1 –M3 (P = 0.001) and i1 –m3 (P <0.001). In all of these craniodental characters, M. fuliginosus is larger than M. phillipsi sp. nov. (Tables 4 and 5). Miniopterus phillipsi sp. nov. also differs significantly from M. fuliginosus in the ratio of tibia to forearm length (TIB/FA; P = 0.002) and the ratio of second phalanx of third digit to third metacarpal (d3mp2/d 3m; P = 0.023). In M. phillipsi sp. nov., TIB/FA ratio is usually higher (median: 42.16%, range: 41.1–43.9%) than in M. fuliginosus (40.78%, 39.6–42.1%), whereas d3mp2/d 3m ratio is lower (83.27%, 79.3–90.4% versus 88.55%, 81.6– 90.9%, respectively). The tragus of M. phillipsi sp. nov. is medium-sized in both length and width. The tragus of M. magnater is longer, broader, and more pointed towards the tip than the other three species in India and Sri Lanka. The middle of the tragus is much broader than its base and tip in M. magnater (slightly broader in M. phillipsi sp. nov.). The tragus of M. fuliginosus has parallel margins along most of its length, as does that of M. pusillus . However, the tragus of M. pusillus is shorter in length and barely curved forward compared to the other three species ( Fig. 8 ).

Description

Miniopterus phillipsi sp. nov. is a medium-sized bat (FA 44–49 mm) exhibiting the typical features of the genus i.e. an elongated second phalanx of the third digit, short and rounded ears, high forehead, short and broad muzzle, and slender and slightly curved tragus with rounded tip (Supplementary Fig. S3 ). Tail length approximately equals head-andbody length ( Table 3 ). The ear is relatively short and rounded (ca. 12 mm in length) and not readily distinguishable from that of M. fuliginosus ( Table 3 ). The tragus is medium sized (5 mm) and slightly curved forward with a rounded tip ( Fig. 8 ). The external measurements of the holotype, paratypes and other specimens of M. phillipsi sp. nov. are given in Table 3 . Fur is dense and soft, fairly long above and short below. Fur slightly extending onto the membranes ventrally, but dorsally confined to the body. The pelage is chocolate-brown above and slightly paler on the under parts (Supplementary Fig. S4 ). Individual hairs are the same color throughout. The skull of M. phillipsi sp. nov. has a wide rostrum and round braincase typical of the genus ( Figs. 5–7 ). Cranial measurements for the holotype and paratypes of M. phillipsi sp. nov. are shown in Table 4. The dentition of M. phillipsi sp. nov. is I 2 /3, C 1/1, P 2/3, M 3/3, which is typical of the genus Miniopterus . Dental measurements of the holotype and paratypes of M. phillipsi sp. nov. are shown in Table 5 .

Natural History

This species is distributed from lower to higher elevations (263–1590 m) of wet and intermediate climatic zones of Sri Lanka. The type locality is the highest elevation it was captured (1590 m); specimens captured at Talawakele (1411 m) document its range in the central highlands of Sri Lanka. Specimens captured at Doteloya were roosting in a granite cave at the edge of a tropical wet lowland rainforest ( Survey Department of Sri Lanka, 2012). Wellawaya and Pallebedda records lie at lower elevations of intermediate climatic zone of Sri Lanka. In western India, it was recorded from Robbers’ Cave, located in the evergreen forest of Mahabaleshwar region of northern Western Ghats at an elevation of 1217 m.

Like other members of this genus, this species apparently prefers to roost in caves and tunnels. Colony sizes of this species are estimated at 1,300 – 1,500 bats in Idulgashinna Cave, 700–1000 bats in Wavulgalge Cave, Wellawaya ( Yapa et al., 2005), 50–100 bats in Sandaraja Cave, Doteloya ( Kusuminda et al., 2020), 200,000 bats in Wavulpane Cave, Pallebedda (Digana, 2004), and 4,200 bats in Robbers’ Cave, Mahabaleshwar ( Korad et al., 2006). Pregnant and lactating females of this species were reported in July and August in Sri Lanka (Digana, 2004; Kusuminda et al., 2018).

holotype,. phillipsi the M

Echolocation calls of recorded M. phillipsi sp. nov. had a mean peak frequency (± SD) of 52.8 kHz ± 0.72 kHz (range: 51–54 kHz, n = 15), which did not differ from those reported for M. fuliginosus from Western Himalaya, India (53.1 kHz in Chakravarty et al., 2020) or from eight colonies in China (53–58 kHz in Zhang et al., 2018). Other Miniopterus originally reported as fuliginosus but presumably pertaining to M. phillipsi sp. nov. include bats from the Western Ghats, India (52.0 kHz in Wordley et al., 2014) and from Kerala, India (53.2 kHz in Srinivasulu and Srinivasulu, 2017). It appears that the new species is not distinguished from M. fuliginosus in echolocation calls.

of of Measurements. Measurements. n size purposes sample and, comparative range for ± SD, shown 0 as are presented Sri Lanka Measurements India and in. Lanka occurring authors Sri different Idulgashinna, of Miniopterus assortment of from species an. by. sp nov and other specimens phillipsi . species other M of new the) mm the while (of, measurements individuals taken by TK

MAW 8.47

8.66 8.77

0.13 21

, 0.12, 14 0.24, 12 0.08 7, 8.1

± 8.9 ± 9.0 ± 9.5 ± – –

– – 8.6 8.4 8.8 8.6 9.2 8.8 8.0 7.9

POB 3.97

3.85 3.95

0.08

, 22 0.05 14, 0.11, 13 0.08 3.7, 7

± – 4.1 ± 4.1 – ± 4.3 – ± –

3.9 3.8 3.9 3.9 4.1 4.0 3.6 3.5

ZYW 8.87

8.65 8.77

0.12

, 9.0

21 0.15 13

9.1,

0.28,

10.0

13 0.09, 7

7.9 ±

–

± – ± ± –

8.7 8.5 8.8 8.6 9.5 9.1 – 7.8 7.7

CIL 14.72

14.82 15.18

0.26 ±, 22 15.6 0.30 ± 15.7 14, ± 0.27 13 16.7, 0.17 ±, 7 13.8 – 14.9 14.5 – 15.1 – 14.8 16.3 – 15.9 13.6 13.4

GSKL 15.23

15.08 15.67

0.24 ± 22, 15.8 ± 0.26 14, 16.4 ± 0.19 13, 17.0 0.22 ± 7 14.5, 15.4 – 14.9 15.8 – 15.3 16.7 16.4 – 14.1 – 13.8

NH

. NH NH taxon 2021.03.01. 2021.03.02. 2021.03.03 all specimens

or Specimen. nov sp

.

other Cranial. and types were 4 T ABLE paratypes. sp. nov

T. Kusuminda, A. Mannakkara, K. D. B. Ukuwela, S. V. Kruskop, C. J. Amarasinghe, et al.

11.05

4.70

7.84 11.28

4.97

8.23

0.18 ± 11.6 22, 0.20 ± 14, 11.9 0.35 ± 13 13.0, ± 0.12 7 10.0, 11.2 – 10.8 11.4 – 11.1 12.4 – 12.0 9.9 9.7 –

0.23 22,

5.4

0.24

6.1

, 14 0.26 12

6.3

, 0.09,

4.5

7

± – ± – ± – ± –

5.1 4.6 5.4 5.0 5.9 5.5 4.4 4.3

0.13

, 22 0.10 14, 0.20 13, 0.19 7, 7.9

± 8.2 – ± – 8.2 ± – 8.7 ± –

8.0 7.8 8.1 7.9 8.5 8.2 7.6 7.3

NMSL, X sp nov.. NMSL, Y nov.. sp, NMSL Y. nov. sp,

phillipsi

.

Holotype. phillipsi Paratype. phillipsi Paratype phillipsi .

fuliginosus . M magnater . M pusillus . M

Figures

FIG. 3. Map of South and Southeast Asia showing sampling localities of M. phillipsi sp. nov. and Miniopterus specimens of mainland Asia mentioned in this study with biomes of ecoregions (Dinerstein et al., 2017). Type locality of M. phillipsi sp. nov. is marked by a black star

FIG. 2. Plot of the first two components of a principal component (PC) analysis for craniodental measurements of the Miniopterus species in India and Sri Lanka (M. philipsii sp. nov. — blue circle; M. fuliginosus — green circle; M. magnater — black circle; M. pusillus — purple circle). Arrow points to holotype. See Table 2 for the variables used in this analysis and the loadings on PC1 and PC2

FIG. 4. Portrait of M. phillipsi sp. nov. NMSL 2021.03.02.NH

FIG. 5. Dorsal aspect of cranium of Miniopterus species in India and Sri Lanka. A — M. magnater (MHNG 1981.071); B — M. fuliginosus (ZMMU S-164504); C — M. pusillus (V/M/ERS/570); D — M. phillipsi sp. nov. (NMSL 2021.03.01.NH, holotype)

FIG. 6. Lateral aspect of cranium and mandible of Miniopterus species in India and Sri Lanka.A — M. magnater (MHNG 1981.071); B — M. fuliginosus (ZMMU S-164504); C — M. pusillus (V/M/ERS/570); D — M. phillipsi sp. nov. (NMSL 2021.03.01.NH, holotype)

FIG. 7. Ventral aspect of cranium of Miniopterus species in India and Sri Lanka. A — M. magnater (MHNG 1981.071); B — M. fuliginosus (ZMMU S-164504); C — M. pusillus (V/M/ERS/570); D — M. phillipsi sp. nov. (NMSL 2021.03.01.NH, holotype)

FIG. 8. Tragus of Miniopterus species in India and Sri Lanka. A — M. magnater (ZMMU S-172585); B — M. fuliginosus (ZMMU S-164505); C — M. phillipsi sp. nov. (NMSL 2021.03.01.NH, holotype); D — M. pusillus (ZMMU S-172595)

Tables

TABLE 3. External measurements (mm) and mass (g) of M. phillipsi sp. nov. from Idulgashinna, Sri Lanka. Measurements presented as 0 ± SD, range, and sample size n. Measurements of the holotype, paratypes and other individuals of the new species and other species of Miniopterus occurring in India and Sri Lanka are shown for comparative purposes. Measurements of M. phillipsi sp. nov. types were taken by TK, while the other specimens by an assortment of different authors

Specimen or taxon	HB	T	HF	TIB	FA	Ear
M. phillipsi sp. nov.	50	55	9.49	19.62	46.71	12.12
Holotype X NMSL 2021.03.01.NH
M. phillipsi sp. nov.	56	56	9.53	20.65	47.52	11.10
Paratype Y NMSL 2021.03.02.NH
M. phillipsi sp. nov.	54	54	8.77	20.05	46.64	11.82
Paratype Y NMSL 2021.03.03.NH
M. phillipsi sp. nov., all specimens	52.0 ± 1.70	53.2 ± 3.25	9.3 ± 0.54	19.7 ± 0.45	46.7 ± 1.05	12.0 ± 0.65
	50–56, 19	48–58, 18	8–10, 19	19–20, 19	44–49, 19	11.1–12.8, 8
M. fuliginosus	55.2 ± 4.74	54.2 ± 5.35	9.2 ± 0.98	19.2 ± 1.21	46.9 ± 2.39	12.3 ± 0.57
	47–63, 10	46–60, 8	7–10, 10	17–20, 9	42–49, 10	11.7–12.9, 4
M. magnater	61.0 ± 2.44	59.0 ± 2.00	9.8 ± 0.56	21.2 ± 0.84	50.5 ± 1.21	12.4 ± 1.18
	56–65, 14	56–64, 15	9–10, 1o	20–22, 1o	48–52, 1o	10.5–14.4, 1o
M. pusillus	48.2 ± 4.64	47.9 ± 2.63	8.1 ± 0.55	17.1 ± 0.78	41.7 ± 0.90	10.4 ± 0.43
	42–57, 9	43–51, 7	7–8, 9	15–17, 9	39–42, 9	10–11, 4