Miniopterus mossambicus, Monadjem & Goodman & Stanley & Appleton, 2013

Monadjem, Ara, Goodman, Steven M., Stanley, William T. & Appleton, Belinda, 2013, A cryptic new species of Miniopterus from south-eastern Africa based on molecular and morphological characters, Zootaxa 3746 (1), pp. 123-142 : 129-139

Miniopterus mossambicus sp. nov.

Mozambique long-fingered bat

Holotype. FMNH 213651 (field number SMG-16875) was collected by Steven M. Goodman and Ara Monadjem on 9 October 2010. This is an adult male fixed in formalin and currently preserved in 70% alcohol. Pectoral muscle was preserved in lysis buffer. The skull has been extracted and cleaned. The specimen has a full adult dentition and the basisphenoid–basioccipital sutures are completely fused. External measurements are: total length 103 mm, tail length 50 mm, hind-foot length (without claw) 6 mm, tragus length 6 mm, ear length 10 mm, and forearm length 41.2 mm. The animal weighed 6.7 g ( Table 3).

Type locality. The specimen was collected in a mist net set over a swimming pool at the Bamboo Inn (15.10306°S; 39.21748°E), along the road to Malawi and on the outskirts of Nampula (town) in the Nampula Province, northern Mozambique, at an altitude of 420 m above sea level .

Etymology. This species is named after the country from which the type series was collected, Mozambique.

Paratype. A second adult male specimen FMNH 213652 (field number SMG-16876) was collected at the same locality and date as the holotype. Both individuals were captured in the same mist net placement, approximately within 15 minutes of one another. Pectoral muscle was conserved in lysis buffer. The skull was not extracted from the specimen. Measurements are provided in Tables 3 .

Specimens referable to Miniopterus mossambicus . The following specimens have not been sequenced and therefore their assignment to M. mossambicus must at present remain tentative; however, morphologically they can be identified as M. mossambicus . All were collected from mid- to high-altitudes in Mozambique and neighbouring Malawi, Zambia and Zimbabwe ( Figure 2 ). Mozambique: DM 8484 and DM 8520 , Gurue Tea Plantation (15° 27.733’S; 37° 01.151’E, altitude 700 m), on 19 and 20 June 2010, respectively ; DM 10836 , Mount Mabu (16° 17.189’S; 36° 24.181’E, altitude 980 m) on 27 November 2008 ; DM 9840 , Manho Forest , Mount Namuli (15° 22.155’S; 37° 03.682’E, altitude 1600 m), date not known. Malawi : BMNH 1987.1178 , Liwonde National Park (15° 02’S; 35° 15’E, altitude 700 m), on 5 June 1985 ; BMNH 1987.1177 and BMNH 1987.1156 , Zomba Plateau (15° 20’S; 35° 19’E, altitude 1800 m), on 23 February and 21 March 1985, respectively. Zambia : BMNH 1968.1014 - 1968.1015 , BMNH 1968.1017 - 1968.1018 , Missale Old Mine (14° 07’S; 32° 52’E, altitude 900 m), between 4 February and 1 May 1963. Zimbabwe : DM 3687 , Umtali (= Mutare) (19° 05’S; 32° 07’E, altitude 1000 m), 17 October 1981. Some of these specimens had previously been assigned to other species : BMNH 1987.1178 – M. schreibersii ( Happold et al. 1987) ; BMNH 1968.1014 - 1968.1018 – M. schreibersii natalensis ( Ansell 1978) ; BMNH 1987.1177 and 1987.1156 – M. fraterculus ( Happold et al. 1987) .

Diagnosis. A small-sized Miniopterus with a forearm length of 41–45 mm. The pelage is grey-brown on the upper and slightly paler on the under parts ( Figure 3 ), with the individual hairs of the under parts having dark bases giving the pelage a bicoloured appearance. Compared with M. natalensis , M. mossambicus is smaller ( Table 3) and has a more gracile skull ( Figures 4 and 5 ). Miniopterus mossambicus has a tragus measuring 5–6 mm that is a relatively thick structure, particular towards the tip and slightly constricted towards the base ( Figure 6 ).

Description. External characters. A relatively small-sized Miniopterus with typical features of the genus including an elongated second phalanx of the third digit. The tail is approximately half the total length ( Table 3). The pelage is grey-brown on the upper and slightly paler on the under parts ( Figure 3 ), with the individual hairs of the under parts having dark bases giving the pelage a bicoloured appearance. The ear is relatively short and rounded (c. 10 mm in length) and not readily distinguishable from other members of the genus in terms of length ( Table 3). The tragus is long (5–6 mm) and largely straight along its length, thickening slightly towards the distal tip and constricting towards the base ( Figure 6 ). The various external measurements of the holotype and paratype of M. mossambicus are given in Table 3.

Cranio-dental characters. The skull of M. mossambicus has a broad rostrum and bulbous braincase typical of the genus ( Figure 7 ). The cranium is intermediate in size compared with the larger M. natalensis and the smaller M. fraterculus , but showing some overlap in measurements with both ( Table 4, Figure 5 ). Similarly, the dental measurements generally fall between those of M. natalensis and M. fraterculus , but with some overlap ( Figure 4 ).

The dentition of M. mossambicus is I 2/3, C 1/1, P 2/3, M 3/3, which is typical of the genus Miniopterus . In the upper tooth row, the inner incisor is larger than the outer one, and the anterior premolar is relatively well developed but with a simple cusp morphology compared with the posterior premolar.

Comparisons. The following taxa of Miniopterus have been described from mainland sub-Saharan Africa, several of which have been placed in synonymy (e.g. Peterson et al. 1995; Simmons 2005), and need to be considered in the description of M. mossambicus sp. nov.: M. africanus Sanborn, 1936 , M. fraterculus , M. inflatus , M. rufus Sanborn, 1936 , M. minor , M. natalensis natalensis , M. natalensis arenarius Heller, 1912 , M. breyeri breyeri Jameson, 1909 , M. breyeri vicinior J. A. Allen, 1917 , M. scotinus (Sandevall, 1846) , M. dasythrix (Temminck, 1840) , M. schreibersii smitianus Thomas, 1927 and M. schreibersii villiersii Aellen, 1956 . Of these, the following species have forearm lengths that are larger than those of M. mossambicus (41.0– 44.9 mm, Table 3): M. africanus (45.4–51.7 mm; Peterson et al. 1995), M. inflatus (46.0– 49.4 mm; Monadjem et al. 2010a); M. rufus (47.4 mm; Sanborn 1936); M. breyeri (46.0 mm; Jameson 1909) or smaller than M. mossambicus : M. minor (38.0– 41.6 mm, Peterson et al. 1995). Two taxa, M. dasythrix and M. scotinus are described from the "Interior of Caffraria", corresponding to the Eastern Cape and Durban (both in South Africa), the terra typica of M. natalensis . This area is outside the known geographic range of M. mossambicus and as M. dasythrix and M. scotinus are probably junior synonyms of M. natalensis , they will not be considered further in these comparisons. Differences between M. mossambicus and the remaining species are discussed below.

Miniopterus fraterculus closely resembles M. mossambicus , especially in overall size and shape (see Table 3). Miniopterus mossambicus has a tragus measuring 5–6 mm, as compared to 4–6 mm in M. natalensis and 4 mm in the holotype and topotype of M. fraterculus (BMNH 5.5.7.18 and 5.5.7.22) ( Goodman et al. 2007). The tragus in M. mossambicus is a relatively thick and linear structure, particular towards the tip and slightly constricted towards the base and is notably more prominent than in M. fraterculus ( Figure 6 ). Furthermore, there is no evidence at present that these two species overlap in distribution (being currently separated by a gap of at least 400 km) ( Figure 2 ). The skull of M. mossambicus is typically more gracile, and the animal is generally smaller in both external and cranio-dental measurements ( Tables 3 and 4) than M. natalensis . While there is considerable overlap of craniodental measurements in univariate space ( Figure 4 ), these two species separate out in multidimensional space ( Figure 5 ). Further, these two taxa show 17.7% genetic divergence ( Table 2). These two species almost certainly overlap in distribution, although the northern limits of M. natalensis are not yet clearly defined ( Monadjem et al. 2010a).

The type specimen of M. natalensis arenarius (USNM 181811) taken at Guaso Nyuki, Kenya, has cranial measurements (GSKL = 14.8 mm, CIL = 14.3 mm) within the range of M. mossambicus , but a larger forearm length (45 mm). The paratype has an even larger forearm length (47 mm). Hence, based on this information, M. n. arenarius has different body proportions to M. mossambicus . Recently, a distinct taxon has been identified from south-western Arabia and Ethiopia which was labelled Miniopterus cf. arenarius ( Sramek et al. 2013) . The authors were unable to confirm whether this species referred to M. arenarius since they did not have comparative material from the type location. We note that M. mossambicus has similar cranio-dental measurements to M. cf. aranerius, but no external measurements were reported for the latter taxon. Since M. mossambicus is clearly distinguishable from the type specimen of M. arenarius based on forearm length, we suspect that it will also be shown to be similarly separable from M. cf. arenarius . If M. cf. arenarius is shown to be distinct from M. arenarius , then it is also probably distinct from M. mossambicus since the distributions of the two species are separated by that of M. arenarius . Therefore, biogeographically, it would be highly unlikely for M. cf. arenarius and M. mossambicus to be conspecific if either was distinct from M. arenarius . The type specimen of M. n. vicinior (AMNH 49019) from Aba, north-eastern DRC, has a forearm length (43.2 mm) within the range of that of M. mossambicus ; however the former taxon is distinctly smaller in dental measurements (C-M 3 = 5.1 mm, C-C = 3.8 mm), which fall within the range of M. minor . The taxon M. s. smitianus is only known from the arid parts of Namibia. The specimens in the BMNH (1935.1.6.44, 1935.9.1.80, 1935.9.1.82) identified as this form had CIL = 14.8–14.9 mm, well outside the range of M. mossambicus (see Table 4). Miniopterus s. villiersii is known from rainforests of Central and West Africa ( Simmons 2005) and, based on the type series, has an overlapping forearm length (44.2–46.0 mm) with M. mossambicus , but larger and non-overlapping GSKL (15.3–15.9 mm) ( Aellen 1956). On the basis of these comparisons, it was possible to eliminate other named taxa of Miniopterus from mainland sub-Saharan Africa as possible candidates for the animals we name here as M. mossambicus .

The PCA analysis showed that morphologically similar or geographically overlapping Miniopterus spp. ( M. minor , M. natalensis and M. fraterculus ), as compared to M. mossambicus , have measurements that occupied different regions of morphospace ( Figure 4 ). The first two axes of the PCA accounted for 90.2% of the total variance ( Table 6). All variable loadings on PC1 were positive indicating a general size vector, whereas PC2 represented a shape vector contrasting high positive (LW) and high negative (UPMOLS, MAND) character loadings ( Table 6). Miniopterus mossambicus occupies a region of morphospace intermediate between M. natalensis and M. fraterculus ( Figure 4 ).

Biology. Miniopterus mossambicus is definitively known from two specimens collected on the outskirts of Nampula, northern Mozambique. However, we have examined 12 other Miniopterus specimens from Mozambique and neighbouring countries that share cranial and dental features with M. mossambicus . We therefore tentatively identify these specimens as M. mossambicus ; the majority of which were collected from highland areas of Mozambique, Malawi and Zimbabwe, although the two type specimens were obtained at lower altitudes.

Miniopterus natalensis in South Africa is known to migrate between high-altitude hibernacula and low-altitude maternity roosts ( van der Merwe 1975). Five of the 14 specimens of M. mossambicus were collected from old mines, indicating that it uses caves as day roosts, typical for the genus ( Monadjem et al. 2010a). The possibility that M. mossambicus employs a similar migratory strategy needs to be investigated. Nothing can be inferred about the reproductive biology of the species.

Release calls were recorded (using an Anabat II bat detector) from a single putative specimen of M. mossambicus captured at Gurue, northern Mozambique (forearm length = 44.0 mm). The frequency of the knee of its echolocation call was 55 kHz, which is similar to that of M. natalensis (55.6 kHz) but significantly lower than that of M. fraterculus (58.4 kHz) from Swaziland ( Monadjem et al. 2010a).

Figures

FIGURE 2. Map of southern Africa showing the type locality for Miniopterus mossambicus sp. nov., as well as localities for the other mainland African specimens mentioned in this study. Miniopterus mossambicus—D; M. fraterculus—•; M. minor— X; M. natalensis—+.

FIGURE 3. Portrait of the holotype of Miniopterus mossambicus sp. nov. (FMNH 213651). (Photograph by Ara Monadjem.)

FIGURE 4. Graph showing width across upper canines plotted against complete upper canine-molar toothrow in different Miniopterus spp. (crosses = M. minor, filled circles = M. fraterculus, open squares = M. mossambicus sp. nov.; plus = M. natalensis). Arrows point to type specimens.

FIGURE 5. A graph plotting the first two components of a principal component (PC) analysis for cranio-dental measurements of the small African Miniopterus species from eastern and southern Africa (crosses = M. minor, filled circles = M. fraterculus, open squares = M. mossambicus sp. nov., plus = M. natalensis). Arrows point to type specimens. See Table 6 for the variables used in this analysis and the loadings on PC1 and PC2.

FIGURE 6. Drawing of the tragus of M. mossambicus sp. nov. holotype (FMNH 213651).

FIGURE 7. Skull of holotype of Miniopterus mossambicus sp. nov. (FMNH 213651). (Photograph taken by John Weinstein, Field Museum image number Z94640_08d.)