Bioacoustics of Myotis (Chrysopteron) nimbaensis

Measurements and craniodental features also distinguish Myotis nimbaensis from M. formosus and M. rufopictus . In terms of measurements, M. nimbaensis is only trivially different or falls within the range of variation in measurements reported for M. formosus (FA = 45.5–53.0 mm; GLS = 17.91–19.45 mm ; ZB = 11.76–12.94 mm ; Csorba et al., 2014 ). However, M. formosus as described by Csorba et al. (2014) can be distinguished based on having a sagittal crest that is missing or only very weakly developed (moderately well developed in M. nimbaensis ), P3 that is not visible in lateral view of the skull (visible in M. nimbaensis ), and a p3 with half the basal area of p2 (p3 is at least three quarters the basal area of p 2 in M. nimbaensis ). In addition, the skull of M. formosus lacks an expanded supraorbital region and appears to have a shorter rostrum than M. nimbaensis when seen in lateral view. Myotis rufopictus (FA = 51.0– 52.5 mm ; GLS = 18.2 mm ; ZB = 11.17; Csorba et al., 2014 ) appears slightly smaller than M. nimbaensis , but both species are known from very few specimens, so the value of this observation is questionable. As described by Csorba et al. (2014) , the skull profile of M. rufopictus ascends almost evenly with no frontal depression (i.e., no clearly defined break between rostrum and sloping forehead as seen in M. nimbaensis ). Like Myotis formosus , M. rufopictus additionally lacks an expanded supraorbital region and it appears to have a shorter rostrum than M. nimbaensis when seen in lateral view. Morphology of P 3 in M. rufopictus is unknown, but p3 is a very small tooth less than one quarter the basal area of p2 and displaced lingually halfway out of the line of toothrow (p3 at least three quarters the area p2 and not displaced in M. nimbaensis ). ECHOLOCATION CALLS: Based on the echolocation calls recorded on the release of the holotype ( n = 22), Myotis nimbaensis emits a broad bandwidth (84.1 ± 13.1 kHz; FMAX: 104 kHz, FMIN: 20 kHz) steep frequency-modulated pulse with a peak frequency of 42.5 kHz (± 4.2 kHz), an average call duration of 3.5 ms (± 0.3 ms), and an interpulse interval of 113 ms (± 5.3 ms; fig. 9). In comparison, echolocation calls of Myotis welwitschii have a lower peak frequency (34 kHz), shorter bandwidth (28.3 kHz) and shorter duration (2.4 ms; Schoeman and Jacobs, 2008: Monadjem et al., 2010 : Collen, 2012 ). While there may be geographic variation in call parameters between East African and Southern African Myotis tricolor populations, calls recorded from Southern Africa have a slightly higher peak frequency (47.8±3.1 kHz) but are shorter in bandwidth (46±23.9 kHz) and duration (3.3±0.6 ms; Schoeman and Jacobs, 2008: Monadjem et al., 2010 ). Echolocation calls of Myotis morrisi are unknown. Myotis bocagii , the other known Myotis species found on the Nimba Mountains, have calls with a similar peak frequency (41–43 kHz) but are shorter in bandwidth (36 kHz) and duration (2–2.8 kHz) (Schoeman and Waddington, 2011; Collen, 2012 ; Monadjem et al., 2017a ).

MOLECULAR ANALYSES: Molecular analyses of mitochondrial cytochrome b sequences from selected specimens ( appendix 2 ) support recognition of Myotis nimbaensis as a distinct species (table 2, figs. 10 and 11). Our analyses recovered well-supported clades consistent with results of Csorba et al. (2014) and Patterson et al. (2019) , and in this context Myotis nimbaensis was found to represent a distinct lineage that nests within the subgenus Chrysopteron as sister to the M. tricolor complex (the clade consisting of M. tricolor 1, 2, and 3 of Patterson et al., 2019 ). Monophyly of Myotis nimbaensis , the M. tricolor complex, and a clade consisting of these two lineages was highly supported (>95% bootstrap). Myotis nimbaensis is 5.18% different than M. tricolor 1, 5.43% from M. tricolor 2, and 5.08% than M. tricolor 3 (table 2). NATURAL HISTORY: The type locality habitat of Myotis nimbaensis occurs at the ecotone of high-altitude grassland, montane savanna, and gallery forest habitats of the Nimba Mountains around 1400 m elevation (fig. 1). As far as is known, the preferred (or exclusive) roosting habitat for this species is subterranean features. The two individuals that we captured were emerging from day roosting in an abandoned mine adit (fig. 1), and echolocation calls similar to the release calls of Myotis nimbaensis recorded at other nearby adits, apparently confirming association of M. nimbaensis with these underground structures. Myotis nimbaensis coroosts with other subterranean roosting bats and was detected at mine adits that house colonies of several hundred Rhinolophus guineensis and Hipposideros lamottei , the latter a bat species endemic to the Nimba Mountains ( Monadjem et al., 2013 ). Foraging habitat for Myotis nimbaensis is unknown, but the six mine adits where M. nimbaensis echolocation calls were recorded occur in similar ecotone habitats at the interface of high-elevation grassland, montane savanna, and gallery forests along headwaters of the Zié, Gouan, and Zougué rivers in the northern Guinean Nimba Mountains.

DIAGNOSIS AND DESCRIPTION: Myotis nimbaensis is diagnosed by a combination of the following characteristics: large size (FA 52.4–55.2 mm , mass 15.5–17.0 g; table 1) with females apparently somewhat larger than males; dorsal fur bright orange with strongly tricolored hairs (basal 1/3 of hair shaft black, middle 1/3 of shaft creamy white, distal 1/3 and tip bright orange to coppery red); ventral fur paler than dorsal fur, tricolored on belly (black base, buff-colored shaft that grades to orange at tip) grading to bicolored (lacking black base) on the sides near the wing membranes; ruff of brighter fur present around neck; pointed face with pale skin covered with orange fur, skin clearly visible through the fur around eye, mouth, and on rostrum; no black spots present on face; pinna with a rounded tip, relatively long and reaching beyond tip of nose when laid forward; pinna with strong distal emargination; skin of pinna pale orange brown becoming slightly darker near the tip, no rim of black around ear; tragus lanceolate, slightly less than half the length of the pinna; thumb brown; wing membranes strongly dichromatic black and orange, with plagiopatagium and dactylopatagium mostly black with narrow bands of orange along the metacarpals, phalanges, and across the membrane behind the forearm and upper arm; black pigmentation extends medially nearly to body and posteromedially to tibia; membrane between metacarpals I and II pale orange; propatagium pale orange; uropatagium orangish brown with orange fur on the proximal 1/3 of the dorsal surface and pale cream-colored fur on proximal 1/5 of ventral surface; no black spots on patagia; no conspicuous gland present in plagiopatagium behind humerus; pale ventral fur extends onto proximal plagiopatagium in narrow strip along body, does not extend past knee; relatively small foot with length approximately 2/5 of tibia length; foot and toes brown, with sparse long brown hairs on the dorsal surface of each toe; wing membrane essentially naked except close to the body, where it has a sparse covering of cream colored hairs on the ventral surface; wing membrane attaches to foot at base of first toe; calcar long, more than twice the length of the hind foot, runs approximately 2/3 of the length of the uropatagium border; skull large for Myotis (GLS = 19.48–19.73 mm ; CIL = 18.92–18.93 mm ; CBL = 18.31–18.81 mm ) with globular braincase, well-defined sloping forehead, and elongated supraorbital region all contributing to the appearance of a clearly defined and elongate rostrum; rostrum with shallow medial depression in nasal region; sagittal crest moderately well developed in both sexes; lambdoid crest weakly developed in both sexes; dental formula I2/3, C1/1, P 3/3, M3/3 = 38; I1 and I2 each with a well-developed posterior cusp; upper canine robust, crown height approximately 2 × that of P4, basal area (as seen in occlusal view) roughly equal to that of P4; anterior two premolars (P2 and P3) much smaller than last premolar (P4); P3 with less than half the basal area of P2 and shifted lingually to be partly excluded from the toothrow although still visible in lateral view; P4 large, sharply pointed, taller than M1; lower incisors each with 4 main cusps; i3 with distal accessory cuspules; p3 relatively large, approximately three quarters the basal area of p2, and fully in line in toothrow, not shifted lingually; lower molars myotodont. COMPARISONS: External and craniodental measurements for Myotis nimbaensis and other congeneric African species with which it might be confused are provided in table 1. In addition to M. nimbaensis , three other large Myotis (subgenus Chrysopteron ) species with orange dorsal fur occur in Africa: M. tricolor , M. welwitschii , and M. morrisi . Descriptions and measurements of these species can be found in Hill and Morris (1971), Hill et al. (1988) , Taylor (2000) , and Monadjem et al. (2010) ; the latter work also includes color photographs and echolocation call spectrograms. Myotis nimbaensis can be easily distinguished from M. morrisi on the basis of size, with M. morrisi being smaller in all external and craniodental dimensions (table 1). The ventral pelage of M. morrisi is also different—rather than being tricolored as in M. nimbaensis , M. morrisi has unicolored dull cream white ventral fur that is tinged a faint brown on the flanks and chin. The skull and dentition of M. morrisi is very similar to that of M. nimbaensis although the braincase of M. morrisi is somewhat more globular and lacks the sagittal crest seen in M. nimbaensis . M. nimbaensis M. morrisi M. tricolor M. welwitschii Malea Femaleb Femalec Malesd Femalese Malef Femaleg M 15.5 17.0 8.0 10.4 (8.5–12.5) 5 10.25 (9.0–12.0) 4 –– TL 111.6 116.3 93.0 108.0 (102.0–116.0) 10 112.4 (104.0–120.0) 10 – 120.0 LT 41.4 46.8 45.0 49.1 (45.0–53.0) 10 52.9 (46.0–61.0) 10 – 55.0 HF 12.0 13.0 10.0 10.3 (9.0–12.0) 9 11.7 (10.0–13.0) 9 – 10.0 Ear 19.5 20.0 16.0 17.8 (15.0–19.0) 10 17.8 (16.0–19.0) 9 – 21.0 FA 52.4 55.2 47.0 48.7 (46.0–50.6) 9 50.3 (48.3–51.6) 10 58.6 55.3 GLS 19.48 19.73 17.01 17.72 (17.11–18.76) 11 18.05 (16.97–18.63) 13 18.94 19.12 CIL 18.93 18.92 16.93 16.82 (15.92–18.07) 10 17.15 (16.09–18.04) 12 18.90 18.60 CBL 18.39 18.81 15.90 16.36 (15.55–17.43) 9 16.70 (15.38–17.94) 13 17.87 17.72 POB 4.75 4.65 3.94 4.38 (3.94–4.64) 12 4.28 (3.91–4.46) 12 5.11 4.84 BB 9.11 9.13 8.07 8.58 (7.84–8.94) 12 8.63 (8.42–8.94) 13 9.33 8.92 MB 9.80 9.86 8.62 9.14 (8.87–9.56) 12 9.31 (9.07–9.58) 12 10.22 9.62 ZB 12.85 12.97 10.60 11.53 (10.84–12.49) 8 11.62 (11.17–12.27) 12 13.14 – MTRL 7.76 7.89 6.80 6.95 (6.60–7.68) 12 6.96 (6.58–7.37) 12 7.82 7.62 BM 8.20 8.26 6.42 7.34 (7.01–7.79) 12 7.44 (7.09–7.80) 13 7.91 8.24 BC 5.44 5.40 4.15 7.71 (4.44–5.13) 10 4.78 (4.57–5.08) 11 – 5.40 a Holotype, AMNH 279589. HF and Ear measurements were taken after preservation. Additional measurement taken in the field: Tibia 22.35, Tragus 9.61. b Paratype, AMNH 279590. HF and Ear measurements were taken after preservation. Additional measurement taken in the field: Tibia 23.28, Tragus 10.62. c Holotype, BMNH 70.488. d AMNH 232029, 232030, 257053; BMNH 14.5.4.2, 64.172, 75.2550, 75.2551, 75.2554, 87.1082; USNM 317927, 317928, 342645, 351061. e AMNH 146789, 257358; BMNH 40.740, 40.741, 75.2549, 75.2552, 75.2553, 75.2555; USNM 292066, 238099, 342634, 242644, 351060. f BMNH 22.12.17.75. g BMNH 22.12.17.76. Myotis nimbaensis is similar in size and general coloration to the widespread species M. welwitschii , but these taxa can be easily distinguished because M. nimbaensis completely lacks the prominent black spots seen on the face and patagia of M. welwitschii (figs. 3–6). Color of the pinnae is also different—bright orange to coppery red with a black edge in M. welwitschii compared to pale orange brown with no black edge in M. nimbaensis . The thumb in M. welwitschii is bright orange whereas it is brown in M. nimbaensis . Both species are strongly dichromatic with black wing membranes and orange along the digits and forearm, but pigmentation of the plagiopatagium near the body and hind legs is different in the two species. Myotis welwitschii has a broad band of orange along the side of the body that extends anteriorly past the elbow to run along the forearm and posteriorly to the ankle, so black pigmentation is limited to the more distal and posterior portions of the plagiopatagium. In contrast, the orange is much less extensive and the black is more extensive in M. nimbaensis ; the black pigmentation approaches the body wall, extending anteriorly into the plagiopatagium behind the humerus and posteriorly to the tibia in M. nimbaensis , so there is no broad band of orange along the body in that species. The uropatagium in M. welwitschii is also bright orange whereas it is darker and more brownish in M. nimbaensis . There are additional differences in features of the dorsal and ventral pelage—the dorsal fur in M. welwitschii is bicolored (black at base and otherwise coppery red) rather than being tricolored as in M. nimbaensis , and M. welwitschii has unicolored ventral pelage (whitish tinged with coppery red) rather than the distinctive tricolored ventral fur in seen in M. nimbaensis . Craniodental measurements (table 1) suggest overall similarity of M. nimbaensis with M. welwitschii ; small differences in a few dimensions are not interpretable given the small sample sizes. Both species have lambdoidal crests that are weakly developed but clearly visible, and moderately well-developed sagittal crests in both sexes. The dentition of M. welwitschii includes two very small anterior upper premolars that are both included in the toothrow; P3 is smaller than P2, but P3 is not displaced lingually as it is in M. nimbaensis .