Miniopterus maghrebensis Puechmaille, Allegrini, Benda, Bilgin, Ibañez & Juste, 2014

Puechmaille, Sebastien J., Allegrini, Benjamin, Benda, Petr, Gürün, Kanat, Šrámek, Jan, Ibañez, Carlos, Juste, Javier & Bilgin, Rasit, 2014, A new species of the Miniopterus schreibersii species complex (Chiroptera: Miniopteridae) from the Maghreb Region, North Africa, Zootaxa 3794 (1), pp. 108-124 : 112-118

Miniopterus maghrebensis Puechmaille, Allegrini, Benda, Bilgin, Ibañez & Juste nov. sp.

Holotype. Adult ♂ ( NMP 94426, field number pb3907 [specimen in alcohol with skull extracted], Kef Azigza Cave , Ksar Tazougart, Morocco, 26 April 2008, leg. P. Benda, J. Červený, A. Konečný and P. Vallo.

Paratypes. 1 ♂ ( EBD 25780 [specimen in alcohol]), Kef Azigza Cave , 30 April 2000, leg. C. Ibáñez, J. Juste, J.A. Garrido and J. Quetglas ;— 4 ♂♂, 7 ♀♀ ( NMP 94506–94512 , 94514 , 94515 [specimens in alcohol with skulls extracted], 94505, 94513 [specimens in alcohol]), Kef Azigza Cave , 26 April 2008, leg. P. Benda, J. Červený, A. Konečný and P. Vallo ;— 1 ♀ ( NMP 90103 [specimen in alcohol with skull extracted]), Oued El Ammar, Sebt-es- Âït-Serhrouchèn , Morocco, 9 September 2003, leg. P. Benda ;— 2 ♂♂ ( NMP 90047 [specimens in alcohol], 90051 [specimen in alcohol with skull extracted]), Oued Tessaoud , Talknout, Morocco, 30 August 2003, leg. P. Benda.

Type Locality. Kef Azigza Cave (or Tazzouguert Cave ), 5.7 km S of Ksar Tazougart, 19 km W-NW of Boudenib, Er Rachidiyah Province, Morocco (32 °01’ 46.6” N, 03° 47’ 16.7” W, 1060 m a. s. l); for a detailed description of the site see Aulagnier and Destre (1985) .

Description and Diagnosis. Miniopterus maghrebensis sp. nov. is a medium-sized member of the genus Miniopterus Bonaparte, 1837 in most respects similar to M. schreibersii (Kuhl, 1817) s.str. ( Figs. 2 , 3 , 4 , 5 ). Forearm length 45–48 mm, condylobasal length of skull 14.7–15.3 mm, zygomatic width of skull 8.4–9.1 mm, length of upper tooth-row (canine to third molar, incl.) 5.7–6.2 mm (for all measurements, n = 25).

The dorsal pelage in M. maghrebensis sp. nov. is chestnut brown to dark greyish-brown, the ventral pelage is pale brown ( Fig. 2 ). Ventral hairs are bicoloured, dark brown on the proximal parts, pale brown to buffy in the distal parts. The dorsal skin of ears and the naked parts of face are pale greyish-brown, the ventral skin of ears is almost without pigments, fleshy pale to pinkish ( Fig. 2 ). Wing membranes are dark brown to dark greyish-brown.

Based on the skull size (cf. Fig. 3 ), M. maghrebensis sp. nov. conforms to the Central European representatives of M. schreibersii s.str., however, is slightly larger than most of the south-European and Levantine specimens, exceeding them on average by ca. 0.3–0.5 mm in largest skull measurements. The rostrum of M. maghrebensis sp. nov. is wide, the width across the infraorbital foramina is large, 4.0– 4.4 mm; the relative width of rostrum (infraorbital width of rostrum / largest length of skull) is very large in comparison to M. schreibersii s.str.: 0.27–0.28 in M. maghrebensis sp. nov. versus 0.24–0.27 in M. schreibersii s.str. from Europe and the Levant. The braincase in M. maghrebensis sp. nov. is high, the height of braincase (incl. the tympanic bullae) 7.7–8.4 mm; the relative height of braincase (largest height of braincase / largest length of skull) is large in comparison to M. schreibersii s.str.: 0.51–0.53 in M. maghrebensis sp. nov. versus 0.45–0.52 in M. schreibersii s.str. from Europe and the Levant. Mandibular molar-row is relatively short in M. maghrebensis sp. nov., its relative length (lower molar-row / mandible length) is 0.326 –0.331 (while 0.336 –0.359 in M. schreibersii s.str. from Europe and the Levant). M. maghrebensis sp. nov. has very distinct tubercle on the dorsal surface of the ramus mandibulae between the third molar and the coronoid process and on the zygomatic arches (cf. Fig. 3 & Šrámek et al., 2013).

*IBP: Interval Between Pulses.

Compared to M. schreibersii s.str. from Europe and the Levant (see Šrámek et al., 2013) unicuspidal teeth are more robust in M. maghrebensis sp. nov. The cingulum on the palatal side of the first upper molar has a very distinctive concave fold between the protoconus and the hypoconus in M. maghrebensis sp. nov.

Measurements of the Holotype (in mm). External: Forearm length 45.8; head and body length 60; tail length 63; ear length 13.4; tragus length 6.3. Cranial: greatest length 15.15; condylobasal length 15.12; zygomatic width 8.59; width of interorbital constriction 3.58; neurocranium width 8.17; neurocranium height 6.31; largest horizontal diameter of tympanic bulla 2.97; rostrum width across upper canines 4.53; rostral width across third upper molars 6.27; length of upper tooth-row (canine to third molar, incl.) 5.93; condylar length of mandible 10.74; coronoid height of mandible 2.57; length of lower tooth-row (canine to third molar, incl.) 6.26.

Genetic Characters. Mitochondrial DNA. The GenBank sequence (partial Cytochrome b, tRNA-Threonine, tRNA-Proline, HV1) of the holotype corresponds to the accession numbers KJ535784 & KJ535824 . M. maghrebensis sp. nov. and M. schreibersii s.str. are sister groups, each species forming a strongly supported monophyletic clade ( Fig. 6 ). The average K2P distance between M. schreibersii s.str. and Miniopterus maghrebensis sp. nov. sequences was 1.2%. Nuclear DNA. The microsatellite data are congruent with the mitochondrial DNA signal and provide clear evidence of two strongly isolated and differentiated gene pools which are represented by Miniopterus schreibersii s.str. and M. maghrebensis sp. nov. ( Figs. 7 & 8 ). The Fst between the Miniopterus maghrebensis sp. nov. and M. schreibersii s.str. colonies ranged between 0.44 and 0.49 (significant values).

Etymology. The name maghrebensis refers to the region (the Maghreb; the region of northern Africa located between the Atlantic Ocean, the Mediterranean Sea, and the Sahara) where the new species was discovered. The proposed vernacular names are Maghrebian bent-wing bat (English), Minioptère du Maghreb (French), Murciélago de cueva magrebí (Spanish), létavec maghrebský (Czech), ặ-----ǘdb*Jl Įặ----×ṣ÷لأ d³ ẕ÷ƆƖ-------è*Jl lỪƖ-------ậķJ (Arabic ⵜ ⵙ ⴰ ⵢ ⵍ ⴰ ⵍ ⴰ ⵎ ⴰ ⴼ ⵔ ⵉ ⵡ ⴻ ⴱ ⵢ ⴻ ⵜ ⵉ ⵏ ⵏ ⵜ ⴼ ⵔ ⵉ ⵇ ⵜ ⵓ ⴳ ⴰ ⴼ ⴰ (Berber).

Distribution. Genetic analyses confirmed its presence from northern Morocco to south of the High Atlas Mountains and northern Tunisia ( Fig. 10 ) ( Šrámek et al., 2013; Puechmaille et al., 2012b; this study); however, these individuals were originally referred to as M. schreibersii . Based on these data and the current extent of Miniopterus distribution in the region ( Aulagnier & Destre, 1986; Kowalski & Rzebik-Kowalska, 1991; Dieuleveut et al., 2010; Puechmaille et al., 2012b), we present a hypothetical distribution map of both species. Nevertheless, all previous records of M. schreibersii from the Maghreb need to be re-evaluated as they could potentially belong to M. maghrebensis sp. nov. since both species are found in the region (Bilgin et al., submitted).

Figures

FIGURE 2. Photographs of Miniopterus maghrebensis sp. nov. individuals from the type locality Kef Azigza Cave, showing the typical appearance of the species. Note that a) was photographed with day light and a flash while b) was photographed during night time with a flash, hence the apparent pelage colour differences (photographs by Jaroslav Červený & Antonín Reiter respectively).

FIGURE 3. Lateral views on skulls and mandibles of Miniopterus maghrebensis sp. nov. and Miniopterus schreibersii (Kuhl, 1817). Legend: a—Miniopterus maghrebensis sp. nov., holotype, NMP 94426, Kef Azigza Cave, Morocco; b—Miniopterus maghrebensis sp. nov., paratype, NMP 94506, Kef Azigza Cave, Morocco; c—M. schreibersii, NMP 94558, Betfia Cave, Romania; d—M. schreibersii, NMP 94560, Betfia Cave, Romania. The arrows point to the very distinct tubercles on the zygomatic arch (top arrow) and on the dorsal surface of the ramus mandibulae of Miniopterus maghrebensis sp. nov. (bottom arrow). Scale bar—5 mm.

FIGURE 4. Occlusal views on the upper tooth-rows of Miniopterus maghrebensis sp. nov. and M. schreibersii (Kuhl, 1817). For legend see Fig. 3. Scale bar—3 mm.

FIGURE 5. Occlusal views on the lower tooth-rows of Miniopterus maghrebensis sp. nov. and M. schreibersii (Kuhl, 1817). For legend see Fig. 3. Scale bar—3 mm.

FIGURE 6. Bayesian consensus tree of mitochondrial DNA showing the phylogenetic relationship between individuals of Miniopterus maghrebensis sp. nov. and M. schreibersii (Kuhl, 1817). Tip of labels are composed of haplotype name followed by the abbreviated two letter country name with the number of samples having this haplotype in square brackets. * HR[2], RO[12], RU[5], SK[8], SI[1], ES[3]. NMP 94426 is the type specimen of Miniopterus maghrebensis sp. nov. Haplotypes from North Africa are in bold face, irrespective of species identity. Abbreviated country names are as follows: AL=Albania, CY=Cyprus, HR=Croatia, ES=Spain, FR=France, LE=Lebanon, MA=Morocco, RO=Romania, RU=Russia, SI=Slovenia, SK=Slovakia, TN=Tunisia, TR=Turkey.

FIGURE 7. Principal component analysis (PCA) showing the clear separation of Miniopterus maghrebensis sp. nov. (filled circles; type specimen NMP 94426 denoted by a "T") and M. schreibersii (Kuhl, 1817) (triangles) based on individuals genotyped at six microsatellite loci. Marks of the same colour indicate individuals sampled at the same location (irrespective of species); Red: Iberia, light blue: Win-Timdouine, dark blue: Talmat, black: Kef Azigza Cave, green: Turkey.

FIGURE 8. Bar plot depicting the posterior probability of assignment of individuals (vertical bars), based on a model-based Bayesian analysis (STRUCTURE), to either M. schreibersii s.str. (green) or Miniopterus maghrebensis sp. nov. (blue). The circle above each bar represents the mitochondrial DNA sequence of the individual grouping in the M. schreibersii s.str. clade (green) or Miniopterus maghrebensis sp. nov. (blue) clade. The individual names followed by the site of origin are presented on the x-axis. WT=Win-Timdouine, ES=Spain, TL=Talmat, KA= Kef Azigza Cave. * type specimen of Miniopterus maghrebensis sp. nov.

FIGURE 10. Hypothetical distribution maps of Miniopterus maghrebensis sp. nov. and M. schreibersii s.str. (Kuhl, 1817). Sites with confirmed species identifications are: 1: Kef Azigza Cave (or Tazzouguert Cave); 2: Oued El Ammar, Sebt-es-Âït- Serhrouchèn; 3: Oued Tessaoud, Talknout; 4: Talmat; 5: Win-Timdouine & Oued Emi Oggoug; 6: Zaghouan mine; 7: Ichkeul National Park; 8: Iberia.