Cryptic diversity in the genus Miniopterus with the description ......FIG.1. Map of southern and eastern Africa showing the distribution of the newly described species, Miniopterus

INTRODUCTION

Small mammals remain poorly known in theAfrotropics (Kingdon et al., 2013), despite thisbeing one of the most diverse regions of the worldfor mammals (Burgin et al., 2018). Indeed, it hasbeen predicted that a greater number of mammalspecies remain to be described in Africa than on anyother continent (Fisher et al., 2018). The number ofnew bat taxa recognized in sub-Saharan Africa con-tinues to rise, with 33 species having been describedor elevated to species rank in the 30 years from 1988to 2018 excluding those described from Madagascarand other offshore islands (Hoffmann et al., 2009;Taylor et al., 2018).

Many of the newly described taxa are crypticspecies, not easily distinguishable based on externalcharacteristics (Monadjem et al., 2013b). The genusMiniopterus appears to be particularly rich in crypticspecies, clearly demonstrated by the rapid increasein the number of recognized species since the appli-cation of molecular techniques to systematic studiesof this group (Goodman et al., 2007, 2009). In 2005,just four species of Miniopterus were recognized onMadagascar (Simmons, 2005); within 10 years thatnumber had risen to 12 species (Christidis et al.,2014; Goodman et al., 2015).

Progress on resolving the taxonomy and system-atics of Miniopterus from mainland Africa has beenfar slower, with only three new species having been

Acta Chiropterologica, 22(1): 1–19, 2020PL ISSN 1508-1109 © Museum and Institute of Zoology PAS

doi: 10.3161/15081109ACC2020.22.1.001

Cryptic diversity in the genus Miniopterus with the description of a new species

from southern Africa

ARA MONADJEM1, 2, 9, JEN GUYTON3, PIOTR NASKRECKI4, 5, LEIGH R. RICHARDS6, ANNA S. KROPFF7, and DESIRE L. DALTON7, 8

1Department of Biological Sciences, University of Eswatini, Private Bag 4, Kwaluseni, Eswatini2Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Private Bag 20, Hatfield 0028,

Pretoria, South Africa3Department of Ecology and Evolutionary Biology, Princeton University, 106A Guyot Hall, Princeton, NJ 08544, USA

4E.O. Wilson Biodiversity Laboratory, Gorongosa National Park, Mozambique 5Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA

6Durban Natural Science Museum, PO Box 4085, Durban 4000, South Africa7South African National Biodiversity Institute, P.O. Box 754, Pretoria, 0001, South Africa

8Department of Zoology, University of Venda, Thohoyandou, South Africa9Corresponding author: E-mail: [email protected]

Species richness in the genus Miniopterus has been greatly under-reported, with a large number of taxa having been discovered anddescribed in the past two decades. Using molecular, standard morphometrics and acoustic data, we present evidence for the existenceof a new species in Mozambique and neighbouring Malawi. Based on cytochrome b (cyt b) and cytochrome oxidase I (COI), thenew species is sister to M. minor, from which it is readily distinguishable by its larger size (including non-overlapping forearmmeasurements, allowing separation in the field). It is distinguishable from sympatric M. mossambicus, itself a newly described taxon from Mozambique, by forearm measurements and a peach-orange wash to the skin around the eyes. In external appearance,it is most similar to M. fraterculus, from which it is only reliably identifiable by multivariate analysis of craniodental features and by a genetic distance of 6.4% in the cyt b gene; the two species also occupy widely differing geographic ranges. The type locality of the new species is Mount Gorongosa, and all known records are from large mountains in central and northernMozambique and southern Malawi. Further research is required to establish its geographic range and understand its basic ecology.Considering its relatively restricted distribution to threatened montane habitats, we suggest that its global conservation status beurgently assessed.

Key words: cryptic species, Miniopteridae, cytochrome b, morphometrics, taxonomy, Mozambique

2 A. Monadjem, J. Guyton, P. Naskrecki, L. R. Richards, and A. S. Kropff

recently described (Monadjem et al., 2013a, 2019;Puechmaille et al., 2014). This is unlikely to be dueto any inherent lack of diversity for biogeographicreasons. On a single mountain in Malawi, south-cen-tral Africa, four Miniopterus species were reported,but none of them could be named with certainty(Curran et al., 2012); this compares well with thesituation in Madagascar where up to four species ofMiniopterus may co-occur (Goodman et al., 2009).Indeed, a recent phylogeny based on a multilocusapproach suggested the existence of up to five unde-scribed taxa in Africa (Demos et al., 2019).

The taxonomy of Miniopterus in West Africa hasrecently been investigated, where currently two spe -cies occur, both endemic to the Upper and LowerGuinea forest block (Monadjem et al., 2019). NorthAfrica also has two species, one of which was re-cently described as a cryptic species (Puechmaille etal., 2014). The situation in East Africa is compli-cated by the lack of recently published surveys, butat least one new species, resulting from the elevationof an existing taxon to specific status, has been un-covered by molecular analysis (Šrámek et al., 2013).Furthermore, the recent multi-locus phylogeny referred to above, demonstrated that nine of the 13 recognized clades of African Miniopterus occurin East Africa (Demos et al., 2019).

Three species have been traditionally recognizedin southern Africa south of the Zambezi River, dif-ferentiated mostly on size (Stoffberg et al., 2004)from smallest to largest: M. fraterculus, M. nata-lensis and M. inflatus (Monadjem et al., 2010b). A fourth species, M. mossambicus, was recently de-scribed from northern Mozambique but was thoughtto extend further south into central Mozambique(Monadjem et al., 2013a) and represents the small-est Miniopterus species in the region. These fourspecies are not easily identifiable in the field but areclearly distinguishable on cranial and genetic char-acteristics (Miller-Butterworth et al., 2005; Mona -djem et al., 2013a), underscoring the fact that cryp-tic species abound in this genus. Adding to theconfusion is the possibility of a fifth species occur-ring in this region, another diminutive species, M. mi nor which is currently known from Tanzania,Central African Republic and Democratic Republicof Congo (Monadjem et al., 2010b), with the west-ern subspecies occidentalis probably a separatespecies (Juste and Ibañez, 1992).

Recent bat surveys on Mount Gorongosarecorded a small Miniopterus species on the mid-slopes of the mountain. Here, we show that this an-imal represents an undescribed taxon, with a larger

distribution closely associated with the high moun-tains of Mozambique and Malawi. Recent studiespoint to this region having a large number of en-demic species (Bayliss et al., 2014; Conradie et al.,2016), many with small distributions centered onone or a few mountains such as the recently de-scribed gecko Afroedura gorongosa (Branch et al.,2017).

MATERIALS AND METHODS

Samples

Bats were captured at Mount Gorongosa (18.48°S, 34.04°E,elevation 920 m above sea level [a.s.l.]) (Fig. 1), and depositedin either the Durban Natural Science Museum, Durban, SouthAfrica (permit information: N/Ref.133/MHN/E.27/2015; 13/1/1/30/2/0-215/08/005246; OP 3321/2015; OP3318/215) or theEO Wilson Laboratory based in Chitengo, Gorongosa NationalPark, Mozambique (permits PNG/DSCi/Cll/2015, PNG/DSCi/C8/2015). Tissue samples were taken from the pectoral musclesof collected specimens.

Genomic DNA Isolation, Amplification andSequencing

Genomic DNA was isolated from tissue samples using theQIAamp DNA Investigator Kit (Qiagen, Germany). Tissue sam-ples were cut with a scalpel blade and were subsequently di-gested overnight (20–22 hours) in Proteinase K and ATL tissuelysis buffer. Following digestion, DNA was isolated accordingto the manufacturer’s instructions. Primers were used to amplifyregions of the mitochondrial genes cytochrome oxidase I (COI,520 bp) and cytochrome b (cyt b, 1140 bp). The COI gene wasamplified using the universal conservative primers BatL5310and R6036R (Hebert et al., 2003). In addition, L14724 andH15915 (Xiao et al., 2001) and L15162 and H15915 (Irwin etal., 1991) were used to amplify a region of cyt b. Amplificationof the respective gene regions was carried out in separate PCRreactions consisting of 1 × DreamTaq Green PCR Master Mix,0.4 µM of each primer, and approximately 20 ng template DNAin a total volume of 20 µl. The temperature profile was as fol-lows: an initial denaturation at 95°C for 2 min, 35 cycles of95°C for 30 s, 55°C for 30 s, and 72°C for 1 min, followed by a final extension at 72°C for 10 min. Successful PCR productswere purified with Exonuclease I and FastAP (Thermo FisherScientific Inc.). Gene fragments were sequenced in both direc-tions using the BigDye Terminator v3.1 Cycle Sequencing Kitand visualized on a 3500 Genetic Analyzer (Applied Biosys -tems). Sequence chromatograms were viewed using SequencingAnalysis Software v.6.0 (ThermoFisher Scientific).

Phylogenetic Analysis

The dataset consisted of 37 cyt b sequences (Table 1), whichcontained 35 reference sequences representing the speciesMiniopterus fraterculus Thomas and Schwann, 1906; M. fuligi-nosus (Hodgson, 1835), M. gleni Peterson, Eger and Mitchell,1995, M. griveaudi Harrison, 1959, M. cf. inflatus, M. macroc-neme Revilliod, 1914, M. majori Thomas, 1906, M. manavi

FIG. 1. Map of southern and eastern Africa showing the distribution of the newly described species, Miniopterus sp. nov., as well asother species mentioned in this study. The location of the type locality is indicated by an arrow, and country names referred to in the

text are provided. Specimens used in the genetic and/or morphological analyses are indicated separately

Cryptic diversity in southern African Miniopterus 3

Thomas, 1906, M. minor Peters, 1857, M. mossambicus Mona -djem, Goodman, Stanley and Appleton, 2013, M. natalensis(A. Smith, 1833), M. orianae Thomas, 1922, and M. sororculusGoodman et al., 2007, obtained from National Center forBiotechnology Information (NCBI) GenBank, Barcode of LifeData System (BOLD) and International Barcode of Life (iBOL).The COI dataset included ten sequences of which eight werereference sequences from M. fuliginosus, M. magnater Sanborn,1931, M. minor, M. cf. natalensis, M. natalensis and M. schrei -bersii (Kuhl, 1817) (Table 2). Lastly, two field isolate sequen-ces (JAG444, JAG445) generated by South African NationalBio diversity Institute (SANBI), and Chaerephon pumilus(Cretzs ch mar, 1826) and Scotophilus dinganii (A. Smith, 1833)were used as outgroups.

All sequences were manually trimmed and aligned withMUSCLE (Edgar, 2004) using default parameters in MEGA 7version 7.0.26 (Kumar et al., 2016). The best model for se-quence evolution, General Time Reversible (GTR) model withGamma distribution (G = 1.53) and Invariable sites (I = 0.58),was determined under the Bayesian Information Criterion (BIC)using the model test function incorporated in MEGA7.Phylogenetic relationships were evaluated using the ML and NJmethod implemented in MEGA 7 (Kumar et al., 2016). To esti-mate support for internal nodes, 1000 bootstrap replicationswere run using the same program (Felsenstein, 1985; Kumar etal., 2016). Sequence variation and average sequence divergencewere determined by group mean distances using the p-distancesubstitution model in MEGA 7 (Kumar et al., 2016). Aligned se-quences were exported to a Fasta file format for BayesianInference (BI) analysis in Mr Bayes (v3.2.7). Markov Chain

Monte Carlo (MCMC) analysis was conducted using the above mentioned model parameters (GTR G+I: nst = 6; rates =invgamma), default parameters for the estimations of priors, onecold and three heated chains, and run for 100,000 generationssampled every 100 generations with a burn in of 25%. By de-fault, two simulations are conducted at the same time. A stoprule parameter using the average standard deviation of split fre-quencies (SD) between the two simulations was also imple-mented to stop analysis when the threshold (SD = 0.01) wasreached, which occurred at 750,000 generations. An SD value of0.05 is the default value used as a diagnostic determinant ofconvergence of the two simulations. An SD value approaching0 indicates that the two simulations become increasingly simi-lar. The generated tree file was converted to the Newick formatusing FigTree (v1.4.3) and annotated in MEGA7. Molecularclock analysis was conducted in BEAST 1.7.4 (Drummond andRambaut, 2007; Drummond et al., 2012) following methods de-scribed in Christidis et al. (2014).

Morphological Analysis

The specimens (listed in Appendix) on which the mor-phometric study is based are deposited in the following collec-tions: The Natural History Museum (formerly The BritishMuseum of Natural History), London (BMNH); Durban NaturalScience Museum (DM); Field Museum of Natural History,Chicago (FMNH); Muséum national d’Histoire naturelle, Paris(MNHN); and E.O. Wilson Biodiversity Laboratory, GorongosaNational Park (EOWL). Measurements of only adult specimens,identified by fully erupted adult dentition and the fusion of

TABLE 1. Cytochrome b (cyt b) sequences of Miniopterus species, and outgroups, used in this study

GenBank No. Species Locality Reference

JAG444 Miniopterus sp. nov. Mozambique This studyJAG445 M. sp. nov. Mozambique This studyAY614744.1 M. natalensis South Africa Miller-Butterworth et al. (2005)KF709542 M. natalensis Namibia Monadjem et al. (2013a)KF709543 M. natalensis Namibia Monadjem et al. (2013a)AY614751.1 M. fraterculus South Africa Miller-Butterworth et al. (2005)AY614754.1 M. fraterculus South Africa Miller-Butterworth et al. (2005)AY614755.1 M. fraterculus South Africa Miller-Butterworth et al. (2005)DQ899760.1 M. fraterculus South Africa Goodman et al. (2007)AY614732.1 M. orianae Australia Miller-Butterworth et al. (2005)KJ535821.1 M. schreibersii Romania Puechmaille et al. (2014)KJ535822.1 M. schreibersii Spain Puechmaille et al. (2014)AY614737.1 M. cf. inflatus Malawi Miller-Butterworth et al. (2005)FJ383129 M. manavi Madagascar Goodman et al. (2009)FJ383130 M. manavi Madagascar Goodman et al. (2009)HQ619934 M. manavi Madagascar Goodman et al. (2011)FJ232797.1 M. griveaudi Anjouan Weyeneth et al. (2008)FJ232798.1 M. griveaudi Comore Weyeneth et al. (2008)FJ383136.1 M. griveaudi Madagascar Goodman et al. (2009)KF709538.1 M. mossambicus Mozambique Monadjem et al. (2013a)KF709539.1 M. mossambicus Mozambique Monadjem et al. (2013a)AY614738.1 M. mossambicus Zambia Miller-Butterworth et al. (2005)AY614739.1 M. mossambicus Zambia Miller-Butterworth et al. (2005)FJ232803.1 M. minor Tanzania Weyeneth et al. (2008)FJ232805.1 M. minor Tanzania Weyeneth et al. (2008)FJ232806.1 M. minor Tanzania Weyeneth et al. (2008)JF440236.1 M. gleni Madagascar Ramasindrazana et al. (2011)JF440237.1 M. gleni Madagascar Ramasindrazana et al. (2011)JF440238.1 M. gleni Madagascar Ramasindrazana et al. (2011)HQ619954.1 M. majori Madagascar Goodman et al. (2011)HQ619955.1 M. majori Madagascar Goodman et al. (2011)HQ619939.1 M. majori Madagascar Goodman et al. (2011)DQ899771.2 M. sororculus Madagascar Goodman et al. (2007)DQ899773.2 M. sororculus Madagascar Goodman et al. (2007)HQ619938.1 M. sororculus Madagascar Goodman et al. (2011)AY614734.1 M. macrocneme New Guinea Miller-Butterworth et al. (2005)AB085735 M. fuliginosus Japan Sakai et al. (2003)AY614756.1 Chaerephon pumilus South Africa Miller-Butterworth et al. (2005)AY614757.1 Scotophilus dinganii South Africa Miller-Butterworth et al. (2005)


the basisphenoid-basioccipital suture, were included in thisstudy. We examined type specimens in the BMNH and FMNH,which included: M. fraterculus (BMNH 1905.5.7.18), M. infla-tus (BMNH 1903.2.4.8, holotype), M. natalensis (BMNH1848.6.12.19, holotype), and M. mossambicus (FMNH 213651,holotype).

The following standard external measurements were taken inthe field: total body length, tail length, ear length, and forearmlength. Forearm length was taken with callipers to the closest 0.1mm; all other measurements were at an accuracy of 1 mm. Bodymass was taken with a Pesola spring balance to the nearest 1 g.

Eight cranial measurements were taken with callipers fol-lowing Monadjem et al. (2013b) that included: greatest skulllength (GSKL), from the posterior-most point of the cranium tothe anterior-most point of the incisors; condylo-incisive length(CIL), from the occipital condyles to the anterior-most point ofthe incisors; greatest zygomatic breadth (ZYGO), the greatestwidth across the zygomatic arches; postorbital width (POB),narrowest dorsal width posterior to the postorbital constriction

of the cranium; greatest mastoid breadth (MAST), greatestbreadth of cranium at mastoid processes; greatest braincasewidth (GBW), lateral braincase width taken posterior to the pos-terior insertion of the zygomatic arches; lachrymal width (LW),greatest width across rostrum at lachrymal projections; andgreatest mandible length (MAND), taken from the posterior-most point of the condylar processes to the anterior-most pointof the incisors.

Eight dental measurements were taken with callipers to theclosest 0.01 mm following Monadjem et al. (2013b) that in-cluded: width across the third molars (M3–M3), taken across theouter-most point of the alveoli of the 3rd molars; completeupper canine-molar tooth row (C–M3), taken from the anterior-most point of the alveolus of the canine to the posterior-mostpoint of the 3rd molar; complete upper tooth row (I1–M3), takenfrom the anterior-most point of the alveolus of the first incisorto the posterior-most point of the 3rd molar; complete uppermolar tooth row (UPMOLS), taken from the anterior-most pointof the alveolus of the anterior premolar to the posterior-most

TABLE 2. Cytochrome oxidase I (COI) sequences of Miniopterus species, and outgroups, used in this study

GenBank No. Species Locality Reference

JAG444 Miniopterus sp. nov. Mozambique This studyJAG445 M. sp. nov. Mozambique This studyKF452626 M. natalensis South Africa S. D. McCulloch, unpublished dataKR259958 M. natalensis South Africa J. Coertse, unpublished dataSKBET039-07 M. cf. natalensis Ethiopia Barcode of Life Data System (BOLD)SKBET028-07 M. cf. natalensis Ethiopia Barcode of Life Data System (BOLD)HQ580335 M. fuliginosus Japan International Barcode of Life (iBOL)KP247545 M. magnater China Li et al. (2015)JF442828 M. schreibersii Russia Kruskop et al. (2012)JF442486 M. minor Kenya B. Agwanda and I. V. Kuzmin, unpublished dataKF452603 Chaerephon pumilus South Africa S. D. McCulloch, unpublished dataMF947528 Scotophilus dinganii South Africa M. Geldenhuys et al., unpublished data


point of the 3rd molar; width across upper canines (C–C), takenacross the outer-most points of the alveoli of the canines; com-plete mandibular molar tooth row (LWMOLS), taken from theanterior-most point of the alveolus of the anterior premolar tothe posterior-most point of the 3rd molar; and complete lowertooth row (i1–m3), taken from the anterior-most point of thealveolus of the first incisor to the posterior-most point of the 3rdmolar. Tooth abbreviations are as follows: I = incisor, C = ca-nine, P = premolar, M = molar; with upper teeth presented inupper case and lower teeth in lower case.

A principal components analysis (PCA) of standardized val-ues of the above craniodental measurements was conducted onthe variance-covariance matrix in package ‘vegan’ (Oksanen etal., 2007) in R version 3.4.4 (R Core Team, 2019), to comparethe morphology of the various taxa measured in this study. Dueto the lack of sexual dimorphism (Monadjem et al., 2010b), thesexes were combined for all analyses.

Acoustic Analysis

Echolocation calls were recorded from hand-released indi-viduals and individuals flying in a large free-flight tent using a full-spectrum recorder Pettersson D1000X at a sampling fre-quency of 300 kHz. Calls were analysed using BatSound Prosoftware (version 3.20 — Pettersson Elektronik, Uppsala,Sweden), and the peak frequency was recorded (Monadjem etal., 2010b).

RESULTS

Molecular Analyses

The phylogenies based on cyt b and COI genesproduced similar tree topologies for both Bayes-ian and neighbor-joining methods (Fig. 2). Basalnodes are poorly supported. However, several clades are apparent. Miniopterus natalensis is sisterto the Malagasy species; embedded within the latter is M. mossambicus. Miniopterus cf. inflatus(from Malawi) is sister to a clade that includes M. fraterculus, M. minor, and the new species from Mount Gorongosa Miniopterus sp. nov. The

new species is sister to M. minor. Genetic distancesbetween the various species mentioned in this phy-logeny were 5–16% (Table 3). The new species M. sp. nov. differs from M. minor between 4.1 and5.7% (average = 4.9%). Divergence based on theBeast analysis (Fig. 3) between M. minor and M. sp. nov. is estimated to have occurred between 1 to 2 Mya.

Morphometric Analyses

A PCA ordination based on craniodental meas-urements showed that southern African Miniopterusspecies mostly occupied distinct morphospace (Fig.4A). The first two principal components accountedfor 92% of the variation, and hence are shown here.The first principal component represented a size gra-dient with highest loadings on GSKL and ZYGO(0.313 and 0.311, respectively), with all other load-ings also being positively associated with it (Table4). As a result, the species are distributed along thisaxis based on size with the smallest species (M. minor) occurring on the left and the largestspecies (M. cf. inflatus) on the right of the ordina-tion. The second principal component representeddifferences in shape with high positive and nega-tive loadings, the largest being with POS and C–M3 (0.440 and -0.493, respectively) (Table 4).Similar sized species were typically separated onthis axis such as M. fraterculus and M. mossambicus(Fig. 4A). Only two species did not separate in mor-phospace: M. mossambicus and the new species M. sp. nov. which overlapped somewhat. How-ever, when these two species (M. mossambicus and M. sp. nov.) were considered separately, theyoccupied non-overlapping areas of morphospace(Fig. 4B), illustrating their distinctiveness in cranialand dental features. Based on these molecular and

FIG. 2. Phylogenetic position of Miniopterus sp. nov. from Mount Gorongosa based on: A — the cyt b gene produced using Bayesiananalysis with posterior probabilities indicated followed by ML bootstrap support; and B — the COI gene produced using NJ analysiswith ML bootstrap support indicated. Labels include accession number, species, and area of collection. * indicates samples sequenced

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morphometric data, we describe a new species ofMiniopterus for Africa.

DESCRIPTION OF NEW SPECIES

Family Miniopteridae Dobson 1875

Genus Miniopterus Bonaparte 1837

Miniopterus wilsoni sp. nov.Wilson’s Long-fingered Bat

HolotypeJAG 444, an adult male, was collected by Jen

Guyton on 22 April 2018, and deposited into the col-lections of the E.O. Wilson Laboratory BiodiversityLaboratory at Chitengo, Gorongosa National Park,Mozambique. The specimen was preserved in 70%ethanol. The skull has been extracted and cleaned.External features of the holotype are illustrated inFig. 5A and its skull in Fig. 6.

Type localityMozambique, Sofala Province, Gorongosa

National Park, Mount Gorongosa (Fig. 1). The batwas collected on 22 April 2018 on Mount Goron -gosa (18.48309°S, 34.04485°W) at 920 m a.s.l. It was netted over a river in a montane riverine for-est fragment adjacent to montane grassland and agri-cultural fields.

ParatypesA single female (JAG 445) was also captured and

collected on the same day at the same site and de-posited into the collections of the E.O. Wilson Labo -ratory Zoological Museum. Photograph of the para -type is illustrated in Fig. 5B.

TABLE 4. Eigenvector loadings of the principal components analysis (PCA) for PC1, PC2, and PC3 based on standardizedcraniodental measurements (see Materials and Methods) of M. sp.nov., M. minor, M. fraterculus, M. natalensis and M. inflatus

Character PC1 PC2 PC3

GSKL 0.313 -0.203 0.085ZYGO 0.311 -0.016 0.310POS 0.290 0.440 0.176MAST 0.304 0.121 0.444GSW 0.306 0.121 0.424C–M3 0.294 -0.493 -0.163C–C 0.297 -0.446 -0.098M3–M3 0.307 -0.259 -0.112MAND 0.303 0.146 -0.265i–m3 0.301 0.206 -0.321LWMOLS 0.291 0.404 -0.517

Cumulative total 88.5 92.1 94.4variation explained (%)

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ion

per

line

age

per

mil

lion

yea

rs


FIG. 4. PCA ordination based on craniodental measurements of: A — all Miniopterus species known to occur in southern Africa; and B — M. wilsoni sp. nov. and M. mossambicus only. For the latter ordination, forearm length was also included

A B


EtymologyThis species is named after Edward O. Wilson

who has supported and facilitated biodiversity re-search at Gorongosa National Park over the pastdecade.

DiagnosisThis is a small-sized Miniopterus currently con-

firmed by molecular analysis from central Mozam -bique, and by morphometric analysis from northernMozambique and southern Malawi. Mean forearmlength for the species is 44.1 mm (n = 8). The smallsize of this bat readily distinguishes it from medium-and large-sized Miniopterus in Africa, particularlythe M. inflatus/M. africanus and the M. natalensisgroups (Happold 2013a, 2013b). In general, M. wil -soni sp. nov. is similar in size to M. fraterculus andM. mossambicus, but significantly larger than thetiny M. minor (Tables 5 and 6); however, in multi-dimensional morphospace based on craniodentalmeasurements, it occupies a distinct morphospace(Fig. 4A and 4B). Furthermore, it can be readily dis-tinguished from sympatric M. mossambicus by fore-arm length (FA > 43 mm in M. wilsoni sp. nov., < 43mm in M. mossambicus); the two species do notoverlap in this measurement (Table 3). Finally, allspecimens of M. wilsoni sp. nov. that have been ex-amined, have a peach-orange wash to the skin of theface under the fur around the eyes, which is absentin M. mossambicus. The only other southern AfricanMiniopterus species with this feature that we areaware of is M. fraterculus, which has a yellowishwash. Morphologically, M. wilsoni sp. nov. most resembles M. fraterculus, from which it differs onmolecular grounds (K2P pairwise genetic distance

6.4%) and on being larger in dental features (Table6). The two species also occupy non-overlappinggeographic ranges. Based on the cyt b gene, the sis-ter species to M. wilsoni sp. nov. is M. minor, fromwhich it can be readily distinguished by its larger,non-overlapping size (forearm length) and mostcraniodental features (Tables 5 and 6).

DescriptionExternal characters. — Miniopterus wilsoni sp.

nov. has the typical features characteristic of thegenus including a rounded head, an elongated sec-ond phalanx of the third digit, rounded ears, and a relatively long and straight tragus (Fig. 5). The tailis almost exactly half that of the total length. Thepelage is medium brown above and only slightlypaler below. Individual hairs are unicoloured. Thespecies is small-sized for a Miniopterus, beinglarger than M. minor, M. occidentalis and M. mos -sam bicus and smaller than M. natalensis and M. cf.inflatus; it does not overlap with any of these fourspecies based on forearm length (Table 3). How-ever, it is similar in size and colouring to that of M. fraterculus. It shares the distinct wash across the face but is peach-orange in colour comparedwith a yellowish wash in M. fraterculus (Fig. 5B).How ever, it is not known whether this is a character specific to these two species, nor whether all indi-viduals of these two species have it. Miniopte-rus wilsoni sp. nov. has a tragus that is mostly equal-ly wide along its entire length, except for a slightconstriction or inflection near its midpoint (Fig. 5B).Unlike M. mossambicus, the tragus of M. wilsoni sp.nov. lacks the slightly constricted base (also evidentin M. fraterculus) and has a rounded tip that is

PC 1 PC 1

PC

2


FIG. 5. Photographs of M. wilsoni sp. nov.: A — in flight showing typical features of the genus; the peach-orange wash to the faceof this species is not obvious in this photograph (holotype, JAG 444); and B — showing the peach-orange wash to the face, and the

relatively long and narrow tragus typical of the genus (paratype, JAG 445) (photographs by Piotr Naskrecki)

A B

broader than the rest of the tragus (Monadjem et al., 2013a).

Craniodental characters. — The skull is gracilefor a Miniopterus species. The rostrum is broad, andthe braincase is rounded and high, typical for thegenus of Miniopterus. The dentition of M. wilsonisp. nov. is I 2/3, C 1/1, P 2/3, M 3/3, which is typicalof the genus. In the upper tooth row, the inner inci-sor is larger than the outer one, and the anterior pre-molar is relatively well developed (Fig. 7). The cra-nial and dental measurements of the holotypecompared with a sample of other southern AfricanMiniopterus species are shown in Table 6.

DistributionCurrently, the only genetically confirmed speci-

mens of this new species come from Mount Goron -gosa, central Mozambique. However, a number ofspecimens collected in northern Mozambique andsouthern Malawi without genetic identification aremorphologically similar and therefore they arelikely to be conspecific with M. wilsoni sp. nov. Allthese specimens were collected on sizeable moun-tains, including Mount Gorongosa (elevation: 1,863m a.s.l.), Mount Namuli (2,419 m a.s.l.), and MountMabu (> 1,600 m a.s.l.) in Mozambique, and ZombaMassif (2,047 m a.s.l.) in Malawi (Fig. 1).

BiologyLittle is known about the biology of this species. It

appears to be associated with montane habitats, withmost records taken from around 1,000 m a.s.l. Basedon our limited sampling, it appears to be the onlyMiniopterus species at higher elevations (> 900 m) onMount Gorongosa. However, two other Miniopterus

species are widely distributed within GorongosaNational Park at lower elevations (< 300 m a.s.l.),M. mossambicus and M. cf. inflatus.

Echolocation calls of specimens captured and re-leased at the same site as the holotype and paratype,and believed to represent the same species, hadmean peak frequency (± SD) of 56.8 kHz ± 0.96kHz (range: 56–58 kHz, n = 4) which is slightlyhigher than that reported for M. mossambicus fromMount Namuli (Monadjem et al., 2013a), howeverthe recordings reported for the latter species weretaken from a location that is now included in the dis-tribution of M. wilsoni sp. nov. and with a differentbat detector (Anabat). The peak frequency of two M. mossambicus in Gorongosa National Park were60 and 61 kHz, while a single individual of thelarger M. cf. inflatus had a peak frequency of 49kHz. Based on these limited recordings, it would ap-pear that the three species of Miniopterus in centralMozambique differ in their echolocation calls.

DISCUSSION

In this paper, we present new information on a population of Miniopterus from Mozambiqueshowing that it represents a new species to science.This is the second new Miniopterus species to be de-scribed from this country in the past decade and fol-lows a trend of new discoveries in Madagascar andWest Africa (Christidis et al., 2014; Goodman et al.,2015; Monadjem et al., 2019). Considering the re-cent phylogeny for Miniopterus by Demos et al.(2019), it would appear that these new species de-scriptions are just the tip of the iceberg, as predictedby Monadjem et al. (2013a).

FIG. 6. The cranium of M. wilsoni sp. nov. (holotype, JAG 444) showing dorsal, ventral, and lateral views of the neurocranium; and lateral view of the mandible (photographs by Piotr Naskrecki). The white grid lines are 1 mm apart



The description of M. wilsoni sp. nov. brings thetotal number of Miniopterus species known fromMozambique to four (Monadjem et al., 2010a,2013a). Within Mozambique, these four species ap-pear to occupy different geographical regions orhabitats. Miniopterus wilsoni sp. nov. is only knownfrom large mountain ranges where it occurs at mid-and perhaps higher elevations. In contrast, M. mos -sambicus and M. cf. inflatus appear to occupy lowerelevations, whereas M. natalensis is only knownfrom the southern parts of the country. All fourspecies also occur beyond the borders of Mozam -bique: with M. natalensis and M. cf. inflatus wide-spread in the region to the south and west of thecountry (Monadjem et al., 2010b); M. mossambicusoccurs further north into Tanzania and Kenya(Demos et al., 2019); and, based on our morpholog-ical analyses, M. wilsoni sp. nov. appears to alsooccur at Zomba Massif, Malawi. Its distribution,however, is not yet fully known and it may occur atother mountains in the region such as MountMulanje (Curran et al., 2012) or perhaps west intoZambia.

Based on the cyt b gene, M. wilsoni sp. nov. ap-pears to have diverged from its closest living rela-tive, M. minor, over the past one to two millionyears. Divergence dates for Miniopterus speciesfrom other regions of continental African have notyet been reported, thwarting any attempts at recon-structing the biogeography of this genus on the con-tinent. However, in Madagascar, there was a pulse ofdiversification between 2–3 Mya, with some taxahaving diverged within the past million years(Christidis et al., 2014). The appearance of M. wil -soni sp. nov., therefore, fits in with the observedtrend of speciation in Malagasy Miniopterus.

It is worth noting that M. cf. inflatus needs nam-ing as it is not conspecific with M. inflatus from cen-tral Africa; in fact, these two taxa belong to differentclades (Monadjem et al., 2019). This species waspreviously thought to be widely distributed acrossAfrica, but recent genetic evidence suggests that it isrestricted to Cameroon and Gabon, although popula-tions in neighboring Congo, Democratic Republic ofCongo and Central African Republic may also referto this species. The West African population has a restricted distribution centered on Mount Nimba(Liberia/Guinea) and surrounding uplands (Mona -djem et al., 2019), while the systematics of the pop-ulations in southern and eastern Africa that werepreviously referred to as ‘M. inflatus’ needs resolv-ing. Furthermore, based on our morphometric analy-ses, M. minor minor from Tanzania is distinguishableS

peci

men

or

taxo

nTo

tal

leng

thTa

il l

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thE

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ody

mas

s

M. w

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–12.

0, 5

10.4

± 1

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8.8

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0, 5

44.1

± 0

.46,

43.

5–44

.9, 8

7.6

± 0

.72,

6.5

–8.5

, 6M

.cf.

infla

tus

112.

4 ±

6.4

6, 1

05–1

20, 5

54.0

± 1

.00,

53–

55, 3

10.5

, 112

.5 ±

0.9

5, 1

1.6–

13.5

, 347

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1.0

4, 4

6.0–

50.0

, 30

14.3

± 1

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8M

. nat

alen

sis

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6, 9

7–10

8, 1

349

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1.8

0, 4

7–52

, 12

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± 0

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, 13

9.8

± 0

.93,

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0, 1

341

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0.7

7, 3

9.8–

42.9

, 18

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± 0

.92,

6.0

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8M

. fra

terc

ulus

100.

7 ±

5.6

8, 8

9–11

0, 1

347

.0 ±

6.1

3, 3

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, 10

8.4

± 0

.81,

7.0

–9.5

, 68.

8 ±

1.3

5, 7

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2.0,

11

43.4

± 0

.87,

41.

4–44

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58.

1 ±

0.9

4, 6

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M. m

inor

90.6

± 3

.21,

83–

99, 3

641

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2.1

1, 3

7–46

, 36

7.8

± 0

.65,

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, 36

10.3

± 0

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10–

11, 3

638

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TA

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ount

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ple

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(in

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lics

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, 13

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± 0

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f. in

flatu

s16

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± 0

.17,

16.

27–1

6.71

, 59.

01 ±

0.1

8, 8

.80–

9.19

, 54.

17 ±

0.1

1, 4

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4.36

, 58.

88 ±

0.1

1, 8

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8.97

, 58.

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0.2

0, 8

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, 512

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± 0

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. nat

alen

sis

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68.

56 ±

0.1

4, 8

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± 0

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0.1

5, 8

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, 16

8.00

± 0

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7.7

2–8.

21, 1

611

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± 0

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10.

74–1

1.74

, 16

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mbi

cus

14.7

1 ±

0.2

4, 1

4.38

–15.

20, 1

78.

06 ±

0.1

8, 7

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8.40

, 83.

77 ±

0.1

3, 3

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4.14

, 17

8.09

± 0

.20,

7.6

0–8.

50, 1

77.

56 ±

0.1

8, 7

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8.00

, 17

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4 ±

0.2

9, 1

0.01

–11.

22, 1

7M

. fra

terc

ulus

14.3

7 ±

0.1

3, 1

4.05

–14.

60, 1

57.

97 ±

0.1

3, 7

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8.20

, 15

3.75

± 0

.10,

3.4

7–3.

87, 1

58.

12 ±

0.1

0, 7

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8.34

, 15

7.46

± 0

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7.2

4–7.

70, 1

510

.39

± 0

.25,

10.

03–1

0.73

, 15

M. m

inor

14.0

7 ±

0.2

5, 1

3.60

–14.

57, 2

17.

62 ±

0.1

6, 7

.35–

7.94

, 21

3.48

± 0

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3.3

2–3.

62, 2

17.

69 ±

0.1

7, 7

.33–

8.03

, 21

7.15

± 0

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6.8

9–7.

42, 2

19.

48 ±

0.2

0, 9

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9.80

, 21

M. o

ccid

enta

lis13

.73

± 0

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13.

45–1

4.00

, 87.

46 ±

0.1

5, 7

.30–

7.80

, 83.

59 ±

0.1

1, 3

.50–

3.75

, 87.

43 ±

0.1

4, 7

.30–

7.70

, 87.

04 ±

0.1

4, 6

.85–

7.30

, 810

.03

± 0

.15,

9.7

0–10

.20,

8

TA

BL

E6.

Cra

nial

and

den

tal

mea

sure

men

ts (

mm

) of

spe

cim

ens

of M

. wils

onis

p. n

ov.

from

Mou

nt G

oron

gosa

, M

ozam

biqu

e. M

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rem

ents

pre

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ed a

s 0

± S

D,

rang

e an

d sa

mpl

e si

ze

(in

ital

ics)

. M

easu

rem

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of

the

holo

type

and

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atyp

e of

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new

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, ot

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fied

as

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ngin

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spe

cies

bas

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n m

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rics

, an

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ies

ofM

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usoc

curr

ing

in s

outh

ern

Afr

ica

are

show

n fo

r co

mpa

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ve p

urpo

ses

Spe

cim

en o

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xon

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3C

–CM

3 –M

3i–

m3

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S

M. w

ilson

isp.

nov

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ype

JAG

444

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5.24

Par

atyp

e JA

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574.

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006.

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ll s

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men

s 5.

55 ±

0.1

9, 5

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5.84

, 13

4.09

± 0

.14,

3.9

0–4.

34, 1

35.

90 ±

0.1

9, 5

.45–

6.13

, 13

6.91

± 0

.19,

6.6

2–7.

31, 1

35.

27 ±

0.1

9, 4

.94–

5.54

, 13

M. c

f. in

flatu

s6.

39 ±

0.0

9, 6

.28–

6.52

, 54.

78 ±

0.1

4, 4

.69–

5.02

, 56.

76 ±

0.0

7, 6

.72–

6.89

, 57.

87 ±

0.1

8, 7

.70–

8.12

, 56.

06 ±

0.2

1, 5

.90–

6.35

, 5M

. nat

alen

sis

5.74

± 0

.10,

5.5

8–5.

93, 1

64.

42 ±

0.1

4, 4

.08–

4.61

, 16

6.29

± 0

.15,

5.8

7–6.

45, 1

67.

54 ±

0.1

7, 7

.26–

7.93

, 16

5.97

± 0

.18,

5.6

8–6.

23, 1

6M

. mos

sam

bicu

s5.

52 ±

0.1

6, 5

.27–

5.87

, 17

4.11

± 0

.13,

3.9

4–4.

40, 1

76.

00 ±

0.1

3, 5

.84–

6.21

, 16

7.10

± 0

.19,

6.9

0–7.

40, 7

5.65

± 0

.18,

5.4

0–5.

80, 7

M. f

rate

rcul

us5.

30 ±

0.0

9, 5

.10–

5.43

, 15

3.90

± 0

.08,

3.7

8–4.

07, 1

55.

65 ±

0.1

1, 5

.50–

5.85

, 15

6.95

± 0

.16,

6.7

0–7.

24, 1

55.

44 ±

0.1

6, 5

.10–

5.66

, 15

M. m

inor

5.25

± 0

.09,

5.0

4–5.

40, 2

13.

95 ±

0.0

9, 3

.79–

4.09

, 21

5.90

± 0

.19,

5.4

5–6.

13, 1

36.

52 ±

0.1

3, 6

.14–

6.88

, 21

4.97

± 0

.09,

4.7

4–5.

14, 2

1M

. occ

iden

talis

5.16

± 0

.09,

5.0

0–5.

30, 8

3.72

± 0

.14,

3.5

0–3.

95, 8

6.76

± 0

.07,

6.7

2–6.

89, 5

6.57

± 0

.25,

6.3

5–7.

00, 8

5.06

± 0

.21,

4.9

0–5.

50, 8

TA

BL

E6.

Ext

ende

d


FIG. 7. Upper teeth of M. wilsoni sp. nov. (holotype, JAG 444) showing: A — the long outer incisors which are almost the same length as the inner incisors; and B — the relatively large anterior premolar (photographs Piotr Naskrecki)

A B


from M. minor occidentalis from Central Afri-can Republic and the Democratic Republic ofCongo, a result mirroring that of Juste and Iba-ñez (1992), and suggesting that these two taxa mayrepresent separate species; this requires further investigation.

The newly described species, M. wilsoni sp. nov.,is only known from relatively high elevations on bigmountains where we assume that it is associatedwith forest edges. The type locality is from mid-elevation riparian forest on Mount Gorongosa whereincreased pressure on the remaining forest frag-ments comes from agriculture and timber harvesting(P. Naskrecki and J. Guyton, personal observation).Such pressure on mid- and high-elevation forests iswell-known on other mountains in the region(Dowsett-Lemaire, 2010; Curran et al., 2012; Bay -liss et al., 2014). Therefore, we suggest that theglobal conservation status of M. wilsoni sp. nov. beassessed without delay, as the chances of it being en-dangered are high.

ACKNOWLEDGEMENTS

We thank Parque Nacional da Gorongosa and theGovernment of Mozambique for permission to conduct this re-search. We thank the Gorongosa Project for facilitating scien-tific research, with special thanks to M. Stalmans, M. Mar ching -ton, R. Pringle, A. G. da Conçeição, Q. Harhoff, M. Jordan, andG. Carr. Funding for J. Guyton’s fieldwork was provided by thePrinceton Department of Ecology and Evolutionary Biology; anNSF Graduate Research Fellowship; National GeographicYoung Explorers Grant 9459-14; the Randall and Mary Hack’69 Award; and Princeton University’s Institutes for AfricanStud ies and International and Regional Studies. The SouthAfrican Department of Agriculture, Forestry and Fisheries andeZemvelo KZN Wildlife are thanked for their assistance withpermitting.

LITERATURE CITED

BAYLISS, J., J. TIMBERLAKE, W. BRANCH, C. BRUESSOW, S. COL -LINS, C. CONGDON, M. CURRAN, C. DE SOUSA, R. DOWSETT,F. DOWSETT-LEMAIRE, et al. 2014. The discovery, biodiver-sity and conservation of Mabu forest — the largest medium-altitude rainforest in southern Africa. Oryx, 48: 177–185.

BRANCH, W. R., J. A. GUYTON, A. SCHMITZ, M. F. BAREJ, P.NASKRECKI, H. FAROOQ, L. VERBURGT, and M.-O. RÖDEL.2017. Description of a new flat gecko (Squamata: Gekkon -idae: Afroedura) from Mount Gorongosa, Mozambique.Zootaxa, 4324: 142–160.

BURGIN, C. J., J. P. COLELLA, P. L. KAHN, and N. S. UPHAM.2018. How many species of mammals are there? Journal ofMammalogy, 99: 1–14.

CHRISTIDIS, L., S. M. GOODMAN, K. NAUGHTON, and B. APPLE -TON. 2014. Insights into the evolution of a cryptic radiationof bats: dispersal and ecological radiation of MalagasyMinio pterus (Chiroptera: Miniopteridae). PLoS ONE, 9:e92440.

CONRADIE, W., G. BITTENCOURT-SILVA, H. M. ENGELBRECHT, S.P. LOADER, M. MENEGON, C. NANVONAMUQUITXO, M.SCOTT, and K. A. TOLLEY. 2016. Exploration into the hiddenworld of Mozambique’s sky island forests: new discoveriesof reptiles and amphibians. Zoosystematics and Evolution,92: 163–180.

CURRAN, M., M. KOPP, J. BECK, and J. FAHR. 2012. Species diversity of bats along an altitudinal gradient on MountMulanje, southern Malawi. Journal of Tropical Ecology, 28:243–253.

DEMOS, T. C., P. W. WEBALA, H. L. LUTZ, J. C. KERBIS PETER -HANS, S. M. GOODMAN, N. CORTES-DELGADO, M. BARTONJO,and B. D. PATTERSON. 2019. Multilocus phylogeny of a cryptic radiation of Afrotropical long-fingered bats (Chi -ro ptera, Miniopteridae). Zoologica Scripta, 49: 1–13.

DOWSETT-LEMAIRE, F. 2010. Further ornithological explorationof Namuli and Mabu Mountains (northern Mozambique),and the urgent need to conserve their forests. African BirdClub Bulletin, 17: 159–177.

DRUMMOND, A. J., and A. RAMBAUT. 2007. BEAST: Bayesianevolutionary analysis by sampling trees. BMC EvolutionaryBiology, 7: 214.


DRUMMOND, A. J., M. A. SUCHARD, D. XIE, and A. RAMBAUT.2012. Bayesian phylogenetics with BEAUti and the BEAST1.7. Molecular Biology and Evolution, 29: 1969–1973.

EDGAR, R. C. 2004. MUSCLE: a multiple sequence alignmentmethod with reduced time and space complexity. BMCbioinformatics, 5: 113.

FELSENSTEIN, J. 1985. Confidence limits on phylogenies: an ap-proach using the bootstrap. Evolution, 39: 783–791.

FISHER, M. A., J. E. VINSON, J. L. GITTLEMAN, and J. M. DRAKE.2018. The description and number of undiscovered mammalspecies. Ecology and Evolution, 8: 3628–3635.

GOODMAN, S. M., K. E. RYAN, C. P. MAMINIRINA, J. FAHR, L. L.CHRISTIDIS, and B. R. APPLETON. 2007. Specific status ofpopulations on Madagascar referred to Miniopterus fra-terculus (Chiroptera: Vespertilionidae), with description of a new species. Journal of Mammalogy, 88: 1216–1229.

GOODMAN, S. M., C. P. MAMINIRINA, N. WEYENETH, H. M.BRADMAN, L. CHRISTIDIS, M. RUEDI, and B. APPLETON.2009. The use of molecular and morphological characters toresolve the taxonomic identity of cryptic species: the case ofMiniopterus manavi (Chiroptera, Miniopteridae). ZoologicaScripta, 38: 339–363.

GOODMAN, S. M., B. RAMASINDRAZANA, C. P. MAMINIRINA, M. C. SCHOEMAN, and B. APPLETON. 2011. Morphological,bioacoustical, and genetic variation in Miniopterus batsfrom eastern Madagascar, with the description of a newspecies. Zootaxa, 19: 1–19.

GOODMAN, S. M., B. RAMASINDRAZANA, K. M. NAUGHTON, andB. R. APPLETON. 2015. Description of a new species of theMiniopterus aelleni group (Chiroptera: Miniopteridae) fromupland areas of central and northern Madagascar. Zootaxa,3936: 538–558.

HAPPOLD, M. 2013a. Miniopterus inflatus Greater long-fingeredbat. Pp. 714–716, in The mammals of Africa. Volume IV:Hedgehogs, shrews and bats (M. HAPPOLD and D. C. HAP -POLD, eds.). Bloomsbury Publishing, London, 800 pp.

HAPPOLD, M. 2013b. Miniopterus schreibersii Schreibers’s long-fingered bat. Pp. 721–722, in The mammals of Africa. Vol -ume IV: Hedgehogs, shrews and bats (M. HAPPOLD and D. C.D. HAPPOLD, eds.). Bloomsbury Publishing, London, 800 pp.

HEBERT, P. D. N., S. RATNASINGHAM, and J. R. DEWAARD. 2003.Barcoding animal life: cytochrome c oxidase subunit 1 di-vergences among closely related species. Proceedings of theRoyal Society, 270B: S96–99.

HOFFMANN, M., P. GRUBB, C. P. GROVES, R. HUTTERER, E. VAN

DER STRAETEN, N. SIMMONS, and W. BERGMANS. 2009. A synthesis of African and western Indian Ocean Islandmammal taxa (Class: Mammalia) described between 1988and 2008: An update to Allen (1939) and Ansell (1989).Zootaxa, 36: 1–36.

IRWIN, D. M., T. D. KOCHER, and A. C. WILSON. 1991. Evolutionof the cytochrome b gene of mammals. Journal of MolecularEvolution, 32: 128–144.

JUSTE, J., and C. IBAÑEZ. 1992. Taxonomic review of Minio pte -rus minor Peters, 1867 (Mammalia: Chiroptera) from westerncentral Africa. Bonner zoologische Beiträge, 43: 355–365.

KINGDON, J., D. HAPPOLD, T. BUTYNSKI, M. HOFFMANN, M.HAPPOLD, and J. KALINA. 2013. Mammals of Africa (6 vol-umes). Bloomsbury Publishing, London, 3760 pp.

KRUSKOP, S. V., A. V. BORISENKO, N. V. IVANOVA, B. K. LIM, andJ. L. EGER. 2012. Genetic diversity of northeastern Palae -arctic bats as revealed by DNA barcodes. Acta Chiro pte ro -logica, 14: 1–14.

KUMAR, S., G. STECHER, and K. TAMURA. 2016. MEGA7: mo-lecular evolutionary genetics analysis version 7.0 for biggerdatasets. Molecular Biology and Evolution, 33: 1870–1874.

LI, S., K. SUN, G. LU, A. LIN, T. JIANG, L. JIN, J. R. HOYT, andJ. FENG. 2015. Mitochondrial genetic differentiation andmorphological difference of Miniopterus fuliginosus andMiniopterus magnater in China and Vietnam. Ecology andEvolution, 5: 1214–1223.

MILLER-BUTTERWORTH, C. M., G. EICK, D. S. JACOBS, M. C.SCHOEMAN, and E. H. HARLEY. 2005. Genetic and Pheno -typic differences between South African Long-fingeredbats, with a global miniopterine phylogeny. Journal ofMam mal ogy, 86: 1121–1135.

MONADJEM, A., M. C. SCHOEMAN, A. RESIDE, D. V. PIO, S. STOFF BERG, J. BAYLISS, P. D. F. COTTERILL, M. CUR-RAN, M. KOPP, and P. J. TAYLOR. 2010a. A recent inventoryof the bats of Mozambique with documentation of sevennew species for the country. Acta Chiropterologica, 12:371–391.

MONADJEM, A., P. J. TAYLOR, F. P. D. COTTERILL, and M. C.SCHO EMAN. 2010b. Bats of southern and central Africa: a biogeographic and taxonomic synthesis. University of theWitwatersrand Press, Johannesburg, South Africa, 596 pp.

MONADJEM, A., S. GOODMAN, W. STANLEY, and B. APPLETON.2013a. A cryptic new species of Miniopterus from south-eastern Africa based on molecular and morphological char-acters. Zootaxa, 3746: 123–142.

MONADJEM, A., L. RICHARDS, P. J. TAYLOR, and S. STOFFBERG.2013b. High diversity of pipistrelloid bats (Vespertilionidae:Hypsugo, Neoromicia, and Pipistrellus) in a West Africanrainforest with the description of a new species. ZoologicalJournal of the Linnean Society, 167: 191–207.

MONADJEM, A. J. T. SHAPIRO, L. R. RICHARDS, H. KARABULUT,W. Y. CRAWLEY, I. B. NIELSEN, A. J. HANSEN, K. BOHMANN,and T. MOURIER. 2019. Systematics of West African Minio -pterus with the description of a new species. Acta Chiro pte -rologica, 21: 237–256.

OKSANEN, J., R. KINDT, P. LEGENDRE, and R. O’HARA. 2007.Vegan: community ecology package. R package version1.9-15. Available at: http://cran.r-project.org (last accessed:1 November 2019).

PUECHMAILLE, S. J, B. ALLEGRINI, P. BENDA, K. GURUN, J. ŠRÁ -MEK, C. IBAÑEZ, J. JUSTE, and R. BILGIN. 2014. A new spe -cies of the Miniopterus schreibersii species complex.Zootaxa, 3794: 108–124.

R CORE TEAM. 2019. A language and environment for statisti-cal computing. Vienna, Austria. Available at www.r-pro-ject.org.

RAMASINDRAZANA, B., S. M. GOODMAN, M. C. SCHOEMAN, andB. APPLETON. 2011. Identification of cryptic species ofMinio pterus bats (Chiroptera: Miniopteridae) from Mada -gascar and the Comoros using bioacoustics overlaid on mo-lecular genetic and morphological characters. BiologicalJournal of the Linnean Society, 104: 284–302.

SAKAI, T., Y. KIKKAWA, K. TSUCHIYA, M. HARADA, M. KANOE,M. YOSHIYUKI, and H. YONEKAWA. 2003. Molecular phy-logeny of Japanese Rhinolophidae based on variations in thecomplete sequence of the mitochondrial cytochrome b gene.Genes and Genetic Systems, 78: 179–189.

SIMMONS, N. 2005. Order Chiroptera. Mammal species of theWorld: a taxonomic and geographic reference, 3rd edition(D. E. WILSON and D. M. REEDER, eds.). Johns HopkinsUni ver sity Press, Baltimore, 2142 pp.

Received 07 December.2019, accepted 31 May 2020

Associate Editor: Wiesław Bogdanowicz


ŠRÁMEK, J., V. GVOŽDÍK, and P. BENDA. 2013. Hidden diversityin bent-winged bats (Chiroptera: Miniopteridae) of theWestern Palaearctic and adjacent regions: implications fortaxonomy. Zoological Journal of the Linnean Society, 167:165–190.

STOFFBERG, S., D. S. JACOBS, and C. M. MILLER-BUTTERWORTH.2004. Field identification of two morphologically similarbats, Miniopterus schreibersii natalensis and Miniopterusfraterculus (Chiroptera: Vespertilionidae). African Zoology,39: 47–53.

TAMURA, K., G. STECHER, D. PETERSON, A. FILIPSKI, and S.KUMAR. 2013. MEGA6: Molecular Evolutionary GeneticsAnalysis version 6.0. Molecular Biology and Evolution, 30:2725–2729.

TAYLOR, P. J., A. MACDONALD, S. M. GOODMAN, T. KEARNEY,

F. P. D. COTTERILL, S. STOFFBERG, A. MONADJEM, M. C.SCHOE MAN, J. GUYTON, P. NASKRECK, et al. 2018. Integra -tive taxonomy resolves three new cryptic species of smallsouthern African horseshoe bats (Rhino lophus). ZoologicalJournal of the Linnean Society, 184: 1249–1276.

WEYENETH, N., S. M. GOODMAN, W. T. STANLEY, and M. RU-EDI. 2008. The biogeography of Miniopterus bats(Chiroptera: Miniopteridae) from the Comoro Archipelagoinferred from mitochondrial DNA. Molecular Ecology, 17:5205–5219.

XIAO, W. H., Y. P. ZHANG, and H. Z. LIU. 2001. Molecular systematics of Xenocyprinae (Teleostei: Cyprinidae): taxon-omy, biogeography, and coevolution of a special group re-stricted in East Asia. Molecular Phylogenetics and Evol -ution, 18: 163–173.


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6.96

5.04

3.98

5.38

9.13

6.36

4.74

min

orF

M 1

9810

5Ta

nzan

iaY

9041

711

374.

5m

inor

FM

198

106

Tanz

ania

X91

439

1039

4.8

13.8

67.

593.

527.

767.

075.

253.

955.

569.

476.

555.

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inor

FM

198

107

Tanz

ania

X91

428

1138

4.8

13.8

87.

463.

507.

617.

205.

183.

805.

529.

36.

465.

06m

inor

FM

198

108

Tanz

ania

Y91

417

1138

4.9

14.0

57.

943.

627.

767.

375.

244.

005.

659.

306.

504.

96m

inor

FM

198

159

Tanz

ania

X88

427

1137

5.2

min

orF

M 1

9816

0Ta

nzan

iaX

8941

810

394.

6m

inor

FM

198

161

Tanz

ania

X83

417

1036

4.1

13.8

77.

593.

417.

547.

025.

384.

025.

519.

426.

605.

00m

inor

FM

198

162

Tanz

ania

Y90

418

1138

5.5

min

orF

M 1

9816

3Ta

nzan

iaX

9141

810

385.

4m

inor

FM

198

164

Tanz

ania

X88

398

1037

5.1

min

orF

M 1

9816

5Ta

nzan

iaY

8937

810

385.

5m

inor

FM

198

166

Tanz

ania

X88

397

1039

5.3

min

orF

M 1

9816

7Ta

nzan

iaX

9041

711

385.

3m

inor

FM

198

168

Tanz

ania

Y87

407

1038

5.1

min

orF

M 1

9816

9Ta

nzan

iaY

9241

810

384.

8m

inor

FM

198

170

Tanz

ania

X91

418

1038

4.7

min

orF

M 1

9817

1Ta

nzan

iaY

9041

910

384.

3m

inor

FM

198

172

Tanz

ania

X91

419

1039

4.2

mos

sam

bicu

sB

M 1

987.

1178

Mal

awi

Y15

.20

8.40

3.80

8.50

8.00

5.40

4.00

5.90

10.8

07.

105.

40m

ossa

mbi

cus

DM

139

13M

ozam

biqu

eX

101

528.

010

.041

.77.

014

.55

8.29

3.74

8.03

7.76

5.62

4.04

5.94

10.9

16.

675.

31m

ossa

mbi

cus

DM

139

14M

ozam

biqu

eX

9748

7.0

9.0

40.6

7.0

14.4

78.

103.

648.

107.

635.

504.

035.

8911

.00

6.82

5.20

mos

sam

bicu

sD

M 1

3936

Moz

ambi

que

Y10

850

8.0

8.0

42.0

8.0

14.7

78.

083.

658.

327.

645.

564.

005.

8410

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6.71

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mos

sam

bicu

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MN

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arat

ype

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que

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047

6.0

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mos

sam

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1365

1H

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ype

Moz

ambi

que

Y10

350

6.0

10.0

41.0

6.7

15.1

27.

923.

738.

187.

535.

784.

295.

9611

.22

7.34

5.77

mos

sam

bicu

sB

M 1

968.

1014

Zam

bia

X14

.50

7.85

3.70

7.60

7.40

5.50

3.95

5.85

10.7

06.

905.

50m

ossa

mbi

cus

BM

196

8.10

15Z

ambi

aX

14.8

08.

103.

708.

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255.

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406.

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mos

sam

bicu

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bia

X14

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7.90

3.60

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11.2

07.

005.

80m

ossa

mbi

cus

BM

196

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18Z

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aX

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08.

103.

708.

007.

605.

504.

206.

1011

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7.00

5.80

mos

sam

bicu

sD

M 3

687

Zim

babw

eY

9947

9.0

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43.0

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14.6

78.

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217.

605.

874.

166.

1611

.07

6.98

5.47

nata

lens

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M 7

190

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109

5611

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.88.

315

.25

8.58

4.10

8.50

8.07

5.85

4.32

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11.4

97.

595.

74na

tale

nsis

DM

791

7E

swat

ini

Y11

252

9.0

10.0

45.5

11.4

15.6

98.

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7.56

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028

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atin

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115

5311

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8.66

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8.58

8.17

5.62

4.61

6.45

11.5

47.

486.

11na

tale

nsis

DM

803

8E

swat

ini

Y11

557

11.0

8.0

45.9

9.6

15.5

08.

544.

018.

688.

215.

934.

466.

3111

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7.79

6.23

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lens

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051

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8.58

8.05

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4.52

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11.3

77.

506.

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tale

nsis

DM

843

0E

swat

ini

Y11

254

10.0

9.0

44.5

11.5

15.5

38.

604.

298.

748.

155.

854.

436.

4511

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7.50

5.94

nata

lens

isD

M 8

433

Esw

atin

iX

112

5511

.010

.046

.610

.515

.45

8.71

4.19

8.68

8.06

5.73

4.33

6.17

11.0

07.

315.

82na

tale

nsis

DM

843

6E

swat

ini

X10

849

11.0

10.0

45.7

11.0

15.4

38.

704.

088.

537.

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684.

526.

4311

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7.54

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nata

lens

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M 8

438

Esw

atin

iY

106

4410

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.411

.015

.21

8.50

4.05

8.40

7.80

5.76

4.50

6.34

11.3

37.

705.

82

AP

PE

ND

IX. C

onti

nued


Taxo

nM

useu

m N

oTy

peC

ount

ryS

exTo

tal

Tail

HF

/cu

Ear

FAM

ass

GS

KL

ZY

GO

PO

BM

AS

TG

BW

C-M

3C

1-C

1M

3-M

3M

AN

Di1

-m3

LWM

OL

S

nata

lens

isB

M 1

848.

6.12

.19

Hol

otyp

eS

outh

Afr

ica

–45

.75.

603.

905.

9510

.60

6.90

6.00

nata

lens

isD

M 1

3288

Sou

th A

fric

aY

106

5210

.010

.645

.811

.815

.66

8.55

4.02

8.50

7.85

5.70

4.44

6.37

11.5

67.

496.

00na

tale

nsis

DM

499

8S

outh

Afr

ica

Y11

147

13.0

12.0

47.5

15.5

78.

683.

998.

618.

125.

854.

546.

4011

.57

7.65

6.11

nata

lens

isD

M 5

529

Sou

th A

fric

aY

104

429.

07.

543

.515

.03

8.23

3.83

8.38

7.72

5.58

4.08

5.87

10.7

47.

935.

88na

tale

nsis

DM

572

9S

outh

Afr

ica

X11

645

.410

.615

.33

8.39

4.09

8.62

7.87

5.74

4.45

6.35

11.4

07.

375.

75na

tale

nsis

DM

680

3S

outh

Afr

ica

X10

748

11.0

9.0

47.8

11.5

15.6

68.

634.

118.

638.

015.

814.

506.

3911

.74

7.45

6.18

nata

lens

isD

M 8

369

Sou

th A

fric

aY

105

4310

.010

.046

.015

.53

8.44

4.18

8.52

7.87

5.74

4.41

6.19

11.5

27.

265.

68na

tale

nsis

DM

837

0S

outh

Afr

ica

Y10

245

11.0

9.0

45.8

15.1

78.

464.

128.

287.

965.

604.

166.

1111

.30

7.49

6.11

occi

dent

alis

MN

HN

198

5-62

8 C

AR

Y13

.60

7.30

3.60

7.30

7.00

5.15

3.70

5.60

10.0

06.

354.

90oc

cide

ntal

isM

NH

N 1

985-

629

CA

RY

13.7

07.

403.

507.

406.

905.

253.

705.

4010

.10

6.40

4.90

occi

dent

alis

MN

HN

198

5-63

1C

AR

Y13

.45

7.40

3.70

7.30

6.85

5.10

3.70

5.50

10.2

06.

705.

00oc

cide

ntal

isM

NH

N 1

985-

637

CA

R–

13.7

57.

403.

507.

507.

105.

303.

505.

1010

.00

6.40

5.20

occi

dent

alis

MN

HN

198

5-64

7C

AR

Y13

.70

7.50

3.50

7.40

7.00

5.10

3.75

5.60

9.70

6.35

5.10

occi

dent

alis

MN

HN

198

5-64

9C

AR

Y13

.90

7.50

3.70

7.50

7.15

5.15

3.95

5.60

10.1

56.

505.

50oc

cide

ntal

isM

NH

N 1

985-

651

CA

RX

14.0

07.

803.

757.

707.

305.

203.

855.

5010

.10

6.85

4.90

occi

dent

alis

BM

195

4.86

6D

RC

Y13

.70

7.40

3.50

7.30

7.00

5.00

3.60

5.40

10.0

07.

005.

00w

ilson

isp.

nov

.B

M 1

987.

1156

Mal

awi

X14

.30

7.50

3.70

7.80

7.30

5.30

3.90

5.90

6.90

5.30

wils

onis

p. n

ov.

BM

198

7.11

77M

alaw

iY

14.7

08.

053.

808.

007.

605.

204.

105.

9010

.80

7.10

5.40

wils

onis

p. n

ov.

DM

108

36M

ozam

biqu

eX

44.9

14.7

07.

843.

628.

027.

585.

694.

125.

8710

.82

6.78

5.10

wils

onis

p. n

ov.

DM

148

47M

ozam

biqu

eX

9951

9.0

10.0

44.0

6.5

14.6

88.

103.

808.

117.

415.

494.

036.

1310

.79

6.77

5.45

wils

onis

p. n

ov.

DM

148

52M

ozam

biqu

eY

101

509.

011

.044

.07.

014

.83

8.05

3.70

8.21

7.76

5.67

4.25

5.78

10.6

76.

955.

54w

ilson

isp.

nov

.D

M 8

484

Moz

ambi

que

Y10

144

.58.

514

.90

8.58

4.04

8.43

7.76

5.84

4.34

6.07

11.1

67.

315.

43w

ilson

isp.

nov

.D

M 8

520

Moz

ambi

que

Y10

443

.58.

014

.43

7.88

3.45

7.57

7.30

5.55

3.90

5.45

10.5

06.

625.

08w

ilson

isp.

nov

.D

M 9

840

Moz

ambi

que

Y7.

78.

843

.714

.37

7.89

3.69

7.95

7.30

5.60

4.09

5.94

10.0

26.

804.

94w

ilson

isp.

nov

.JA

G44

4H

olot

ype

Moz

ambi

que

Y95

449.

010

.044

.27.

815

.10

8.23

3.88

8.23

7.69

5.63

4.16

6.00

10.6

16.

955.

24w

ilson

isp.

nov

.JA

G44

5P

arat

ype

Moz

ambi

que

X92

459.

012

.043

.77.

514

.86

8.00

3.67

8.28

7.58

5.57

4.03

6.00

10.5

46.

905.

19

AP

PE

ND

IX. C

onti

nued

Documents

Cryptic diversity in the genus Miniopterus with the description ......FIG.1. Map of southern and eastern Africa showing the distribution of the newly described species, Miniopterus