Miniopterus nimbae, Monadjem & S Hapiro & Richards & Karabulut & Crawley & Nielsen & Hansen & Bohmann & Mourier, 2019

Monadjem, Ara, Shapiro, Julie T., Richards, Leigh R., Karabulut, Hatice, Crawley, Wing, Nielsen, Ida Broman, Hansen, Anders, Bohmann, Kristine & Mourier, Tobias, 2019, Systematics of West African Miniopterus with the description of a new species, Acta Chiropterologica 21 (2), pp. 237-256 : 245-248

Miniopterus nimbae sp. nov.

Nimba long-fingered bat

Holotype

DM 12621 (field no. AM2010_12_18_1 ), an adult male, was collected by Ara Monadjem. The specimen was fixed in formalin and then transferred to 70% alcohol. The skull has been extracted and cleaned. Photograph of the skull and drawing of the tragus of the holotype are illustrated in Figs. 6 and 7 .

Type locality

Liberia, Nimba Province, Mount Gangra, 10 km to the west of Mount Nimba ( Fig. 1 ). The bat was netted on 18 December 2010 exiting from a mine adit mid-way up Mount Gangra (7.55434°N, 8.62902°W) at 720 m a.s.l, in secondary forest.

Paratypes

No other specimens of this species were captured or collected on the same day at the same site. However, the previous night an adult female (DM 12614) was collected at the Yiti River 9 km to the south-east of Mount Gangra. Photograph of the paratype is illustrated in Fig. 8 .

Etymology

This species is named after Mount Nimba, one of just three localities from which it is known, further highlighting the critical importance of this mountain for bat conservation in Africa ( Monadjem et al., 2016).

Diagnosis

This is a large-sized Miniopterus from Mount Nimba, Liberia, with a mean forearm length of 47.4 mm (n = 26 individuals). The large size of this bat (particularly its forearm length) readily distinguishes M. nimbae from all other African Miniopterus taxa except the M. inflatus / M. africanus group. In external and craniodental measurements, M. nimbae is similar in size to other members of the M. inflatus group ( M. inflatus s.s., M. cf. inflatus and M. africanus ) (Tables 3–5); however, in multi-dimensional morphospace based on craniodental measurements, it overlaps only with M. inflatus s.s. The taxon M. cf. inflatus from eastern and southern Africa tends to have a light pelage, being more reddish-brown in colour (compared with a deep chocolate brown in M. nimbae ).

It is not possible, at present to distinguish M. nimbae from M. inflatus s.s. on external characters. However, they can be readily distinguished by cranial features. In particular, the 1st upper premolar has an additional lingual cusp, posterior to the main cusp, that is present in M. nimbae but absent in M. inflatus s.s. ( Fig. 9 ); this feature being clearly visible, even with a low magnification hand lens, and consistently present in all the specimens examined in this study. The lower tooth row (i 1 –m 3) and lower molar (LWMOLS) lengths are also slightly larger in M. nimbae than M. inflatus s.s. In terms of cranial geometry, M. nimbae differs from M. inflatus s.s. as it bears a slightly more gracile skull, less ‘inflated’ braincase, and the point of maximum curvature along the occiput is more elevated in the newly described taxon than in the nominate form. Furthermore, these two taxa, are also distinguishable on molecular grounds (K2P pairwise genetic distance = 1.6%). Additionally, the ranges of the two taxa do not appear to overlap. Miniopterus africanus appears to be restricted to north-eastern Africa and is genetically distinct (K2P pairwise distance = 16.7%) from M. nimbae .

Description

External characters.— Miniopterus nimbae is large-sized for the genus, but showing typical generic features including a rounded head, an elongated second phalanx of the third digit, rounded ears, and a relatively long and straight tragus. The tail is slightly less than half that of the total length. The pelage is dark chocolate brown above and slightly paler below. Individual hairs are unicoloured. The mass and standard external measurements of the holotype compared with a small sample of other individuals are shown in Table 3.

Craniodental characters.—The skull is robust for a Miniopterus species. The rostrum is broad and the braincase is rounded and high, typical for the genus of Miniopterus . The dentition of M. nimbae is I 2/3, C 1/1, P 2/3, M 3/3, which is typical of the genus. In the upper tooth row, the inner incisor is larger than the outer one, and the anterior premolar is relatively well developed. The cranial and dental measurements of the holotype compared with a small sample of other individuals are shown in Tables 4 and 5.

Distribution

Analysis of genetic samples taken from five specimens with large forearm lengths (range 46.9– 48.2 mm) at Mount Gangra (Nimba, Liberia), group them all as M. nimbae ( Figs. 2 and 3 ). Although not genetically analysed, it is likely that specimens previously collected from northern Liberia or southeastern Guinea and identified as M. inflatus are instead referable to this new species, M. nimbae . Based on this assumption, this taxon is known from just three localities: Mount Nimba (and surrounding uplands), Liberia; Wonegizi Mountains, Liberia; and Mount Béro, Guinea ( Wolton et al., 1982; Koopman et al., 1995; Fahr et al., 2006; Monadjem et al., 2016). The closest locality for M. inflatus s.s. is at least 2,000 km away in eastern Nigeria ( Happold, 2013 b), and no other large Miniopterus specimens have been collected in the intermediate area, despite extensive surveys in a number of localities e.g., Thaï and Comoé National Parks in Côte d’Ivoire ( Fahr and Kalko, 2011), the Simandou Range in eastern Guinea ( Decher et al., 2015), the Fouta Djallon mountains in central Guinea ( Weber and Fahr, 2007) or anywhere in Ghana or Sierra Leone ( Grubb et al., 1998; Happold, 2013 b, 2013 c). Therefore, M. nimbae is probably an endemic to the upland areas of northern Liberia and south-eastern Guinea, and may be shown to also occur in the upland area of western Côte d’Ivoire at and around Mount Nimba.

Biology: Practically nothing is known about the biology of this Upper Guinea forest endemic. It has been recorded roosting in mine adits at 720– 970 m above sea level (a.s.l.) at Mount Gangra and Mount Yuelliton (both within 10 km of Mount Nimba). The size of one roosting colony at Mount Gangra was estimated at between 20–30 individuals; the site was shared with large numbers of Myonycteris angolensis and Hipposideros cf. ruber , and a few H. marisae . A second roosting colony was estimated to include> 200 individuals of this species at Mount Yuelliton (which was not inhabited by any other bat species — A. Monadjem, personal observation). It has been netted at various localities in the foothills of Mount Nimba and in the low-lying rainforest region between these three upland areas. This suggests that this species roosts in upland areas (700 m a.s.l.), and then descends to forage in lower lying forested areas (about 500 m a.s.l.). In a sample of 13 females captured at Nimba between late December and end-March, five were pregnant. During the same period, three out of 10 males had scrotal testes. The mean frequency of the knee of handreleased M. nimbae captured at Mount Nimba was 48.4 kHz (range: 47.2–48.9 kHz, n = 4).

Other Taxonomic Considerations

In addition to the description of the new species, M. nimbae , the phylogeny presented here ( Figs. 2 and 3 ) also identifies two other distinct taxa. The first is the taxon M. villiersi , which does not appear to be closely related to M. schreibersii s.s. and should therefore not be considered a subspecies of the latter mentioned taxon. In fact, M. villiersi is sister to M. nimbae ( Figs. 2 and 3 ), from which it is readily distinguishable based on genetics and size (see Tables 2–5); the pairwise genetic distance between the two species is 9.0%, and there is no overlap between these two species in forearm length or any of the craniodental measurements presented here. The echolocation calls also differ, with the frequency of the knee of M. villiersi calls (based on hand-released individuals that were captured at Mount Nimba — x = 51.6 kHz, range 51.1–52.4 kHz, n = 5) being distinctly higher than that of M. nimbae (x = 48.4 kHz, range 47.2–48.9 kHz, n = 4) with no overlap between the two species.

The second taxon refers to the M. inflatus group, which appears to be paraphyletic. Miniopterus inflatus s.s. (based on sequenced specimens from Gabon, and close to the type locality in southern Cameroon) is sister to the taxon M. nimbae and these two are sister to M. villiersi ( Figs. 2 and 3 ). By contrast, the M. cf. inflatus specimens (from Malawi and Mozambique) are sister to M. fraterculus and M. minor . This suggests that the taxon M. inflatus s.l. comprises, in addition to the newly recognised M. nimbae , two distinct and not closely related taxa which we refer to as M. inflatus s.s. (from Gabon), and M. cf. inflatus (from Malawi and Mozambique).

Figures

FIG. 6. Skull and mandible of the paratype (left) and holotype (right) of M. nimbae sp. nov. (DM 12614 and DM 12621, respectively) in dorsal, ventral, and lateral view. Scale bars = 10 mm

FIG. 7. Drawing of the tragus of the holotype of M. nimbae sp. nov. as well as the tragi of selected African Miniopterus species: A — M. nimbae sp. nov. (DM 12621); B — M. villiersi (DM 14185); C — M. inflatus s.s. (Gabon) (DM 14078); D — M. cf. inflatus (Mozambique) (DM 8556)

FIG. 1. Map showing the type and sampling localities of Miniopterus taxa on mainland Africa (including Sao Tomé Island) referred to in this study, arranged by body size class; A — Large-sized species: M. nimbae sp. nov. (circles), M. inflatus (squares), M. cf. inflatus (pentagons), and M. africanus (triangles); B — Medium-sized species: M. villiersi (circles), M. natalensis (squares), M. n. arenarius (triangles), and M. maghrebensis (pentagons); and C — Small-sized species: M. mossambicus (circles), M. minor (triangles), M. newtoni (squares), and M. fraterculus (pentagons). Filled symbols refer to those specimens used for both molecular and morphological analysis, unfilled symbols refer to those only used in the molecular analysis, and symbols with a dot refer to those only used in the morphometric analysis. The star symbols show the type locality of the taxa referred to in this study (names of taxa placed above and to the right)

FIG. 8. Lateral view portrait of the paratype of M. nimbae sp. nov. (DM 12614) showing the typical rounded head of Miniopterus species (photograph by AM)

FIG. 9. Ventral view of the 1st premolar on the left side of the upper jaw in: A — M. nimbae sp. nov. (DM 12621); B — M. villiersi (DM 14185); C — M. inflatus s.s. (Gabon) (DM 14078); D — M. cf. inflatus (Mozambique) (DM 8556). The arrows point to this cusp on the 1st upper premolar in M. nimbae or to its absence in the other species

FIG. 2. Phylogeny based on Neighbour-joining tree. Bootstrap support from 1000 replicates indicated on branches

FIG. 3. Phylogeny based on Bayesian tree with posterior probabilities shown on branches