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A new species of the Miniopterus schreibersii species complex (Chiroptera: Miniopteridae) from the Maghreb Region, North Africa



We used an integrative approach combining cranio-dental characters, mitochondrial and nuclear data and acoustic data to show the presence in the genus Miniopterus of a cryptic species from the Maghreb region. This species was previously recognised as Miniopterus schreibersii (Kuhl, 1817). Miniopterus maghrebensis sp. nov. can be differentiated from M. schreibersii sensu stricto on the basis of cranial characters and from mitochondrial DNA and microsatellite evidence. Although slight external morphological and acoustic differences were noted between the two species, these criteria alone did not allow reliable species identification from live animals. Based on the specimens identified morphologically and/or genetically, the distribution range of M. maghrebensis sp. nov. extends from northern Morocco to south of the High Atlas Mountains and northern Tunisia. The new cryptic species is found in sympatry with M. schreibersii s.str. near coastal regions of North Africa.


Bats, cryptic species, echolocation, Mammalia, Morocco

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Ansell, W.F.H. & Topál, G. (1976) The type locality of Miniopterus schreibersi (Kuhl) (Mammalia: Chiroptera). Vertebrata hungarica Musei historico-naturalis hungarici, 17, 15–18.

Arlettaz, R. (1999) Habitat selection as a major resource partitioning mechanism between the two sympatric sibling bat species Myotis myotis and Myotis blythii. Journal of Animal Ecology, 68 (3), 460–471.

Arlettaz, R., Christe, P., Lugon, A., Perrin, N. & Vogel, P. (2001) Food availability dictates the timing of parturition in insectivorous mouse-eared bats. Oïkos, 95, 105–111.

Aulagnier, S. & Destre, R. (1985) Introduction à l'étude des Chiroptères du Talifat (sud-est marocain). Mammalia, 49 (3), 329–337.

Aulagnier, S. & Destre, R. (1986) Les chiroptères du sud-marocain : notes éco-éthologiques et biogéographiques. In: Les chiroptères : Colloque francophone de mammalogie. Société française pour l’étude et la protection des mammifères, Rouen, pp. 123–129.

Baker, R.J. & Bradley, R.D. (2006) Speciation in Mammals and the genetic species concept. Journal of Mammalogy, 87 (4), 643–662.

Barataud, M. (2012) Ecologie acoustique des chiroptères d'Europe. Identification des espèces, étude de leurs habitats et comportements de chasse (Biotope ed.). Mèze & Paris, 344 pp.

Benda, P., Hulva, P. & Gaisler, J. (2004a) Systematic status of African populations of Pipistrellus pipistrellus complex (Chiroptera: Vespertilionidae), with a description of a new species from Cyrenaica, Libya. Acta Chiropterologica, 6 (2), 193–217.

Benda, P., Kiefer, A., Hanák, V. & Veith, M. (2004b) Systematic status of African populations long-eared bats, genus Plecotus (Mammalia: Chiroptera). Folia Zoologica, 53 (Monograph 1), 1–47.

Benda, P. & Vallo, P. (2012) New look on the geographical variation in Rhinolophus clivosus with description of a new horseshoe bat species from Cyrenaica, Libya. Vespertilio, 16, 69–96.

Berthier, P., Excoffier, L. & Ruedi, M. (2006) Recurrent replacement of mtDNA and cryptic hybridization between two sibling bat species Myotis myotis and Myotis blythii. Proceedings of the Royal Society of London, B, 273 (1605), 3101–3109.

Bilgin, R., Gürün, K., Maraci, Ö., Furman, A., Hulva, P., Çoraman, E., Lučan, R.K., Bartonička, T. & Horáček, I. (2012) Syntopic occurrence in Turkey supports separate species status for Miniopterus schreibersii schreibersii and M. schreibersii pallidus (Mammalia: Chiroptera). Acta Chiropterologica, 14 (2), 279–289.

Bilgin, R., Maracı, Ö., Gürün, K., Rebelo, H., Puechmaille, S.J., Presetnik, P., Hamidovic, D., Fressel, N., Hulva, P., Horáček, I., Ibañez, C., Karataş, A., Karataş, A., Allegrini, B., Georgiakakis, P., Gazaryan, S., Nagy, Z., Abi-Said, M., Lučan, R.K., Bartonička, T., Nicolaou, H., Scaravelli, D., Karapandža, B., Uhrin, M., Paunović, M., Benda, P. & Juste, J. (submitted) Circum-Mediterranean phylogeography of a bat coupled with past environmental niche modelling: a new paradigm for the recolonization of Europe? Molecular Ecology.

Brito, J.C., Godinho, R., Martínez-Freiría, F., Pleguezuelos, J.M., Rebelo, H., Santos, X., Vale, C.G., Velo-Antón, G., Boratyński, Z., Carvalho, S.B., Ferreira, S., Gonçalves, D.V., Silva, T.L., Tarroso, P., Campos, J.C., Leite, J.V., Nogueira, J., Álvares, F., Sillero, N., Sow, A.S., Fahd, S., Crochet, P.-A. & Carranza, S. (2014) Unravelling biodiversity, evolution and threats to conservation in the Sahara-Sahel. Biological Reviews, 89 (1), 215–231.

Castella, V., Ruedi, M., Excoffier, L., Ibañez, C., Arlettaz, R. & Hausser, J. (2000) Is the Gibraltar strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertilionidae)? Molecular Ecology, 9, 1761–1772.

Clare, E.L., Lim, B.K., Engstrom, M.D., Eger, J.L. & Hebert, P.D.N. (2007) DNA barcoding of Neotropical bats: species identification and discovery within Guyana. Molecular Ecology Notes, 7, 184–190.

Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9 (8), 772–772.

Davidson-Watts, I., Walls, S. & Jones, G. (2006) Differential habitat selection by Pipistrellus pipistrellus and Pipistrellus pygmaeus identifies distinct conservation needs for cryptic species of echolocating bats. Conservation Biology, 133, 118–127.

Dietz, C., von Helversen, O. & Nill, D. (2009) Bats of Britain, Europe & Northwest Africa. London: A & C Black Publishers Ltd., 400 pp.

Dieuleveut, T., Lieron, V. & Hingrat, Y. (2010) Nouvelles données sur la répartition des Chiroptères dans le Maroc oriental (années 2007 à 2009). Bulletin de l'Institut Scientifique, Rabat, section Sciences de la Vie, 32 (1), 33–40.

Dool, S.E., Puechmaille, S.J., Dietz, C., Juste, J., Ibáñez, C., Hulva, P., Roué, S.G., Petit, E.J., Jones, G., Russo, D., Toffoli, R., Viglino, A., Martinoli, A., Rossiter, S.J. & Teeling, E.C. (2013) Phylogeography and postglacial recolonization of Europe by Rhinolophus hipposideros: evidence from multiple genetic markers. Molecular Ecology, 22 (15), 4055–4070.

Douangboubpha, B., Bumrungsri, S., Soisook, P., Murray, S.W., Puechmaille, S.J., Satasook, C., Bu, S.S.H., Harrison, D.L. & Bates, P.J.J. (2010) A taxonomic review of Hipposideros halophyllus, with additional information on H. ater and H. cineraceus (Chiroptera: Hipposideridae) from Thailand and Myanmar. Acta Chiropterologica, 12 (1), 29–50.

Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.

Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164, 1567–1587.

Flanders, J., Jones, G., Benda, P., Dietz, C., Zhang, S., Li, G., Sharifi, M. & Rossiter, S.J. (2009) Phylogeography of the greater horseshoe bat, Rhinolophus ferrumequinum: contrasting results from mitochondrial and microsatellite data. Molecular Ecology, 18, 306–318.

Francis, C.M., Borisenko, A.V., Ivanova, N.V., Eger, J.L., Lim, B.K., Guillen-Servent, A., Kruskop, S.V., Mackie, I. & Hebert, P.D. (2010) The role of DNA barcodes in understanding and conservation of mammal diversity in southeast Asia. PLoS One, 5 (9), e12575.

Furman, A., Öztunç, T. & Çoraman, E. (2010) On the phylogeny of Miniopterus schreibersii schreibersii and Miniopterus schreibersii pallidus from Asia Minor in reference to other Miniopterus taxa (Chiroptera: Vespertilionidae). Acta Chiropterologica, 12 (1), 61–72.

Garcia-Mudarra, J.L., Ibañez, C. & Juste, J. (2009) The straits of Gibraltar: barrier or bridge to Ibero-Moroccan bat diversity? Biological Journal of the Linnean Society, 96, 434–450.

Goodman, S.M., Maminirina, C.P., Bradman, H.M., Christidis, L. & Appleton, B.R. (2010) Patterns of morphological and genetic variation in the endemic Malagasy bat Miniopterus gleni (Chiroptera: Miniopteridae), with the description of a new species, M. griffithsi. Journal of Zoological Systematics and Evolutionary Research, 48 (1), 75–86.

Goodman, S.M., Maminirina, C.P., Weyeneth, N., Bradman, H.M., Christidis, L., Ruedi, M. & Appleton, B. (2009) The use of molecular and morphological characters to resolve the taxonomic identity of cryptic species: the case of Miniopterus manavi (Chiroptera, Miniopteridae). Zoologica Scripta, 38 (4), 339–363.

Gunnell, G.F., Eiting, T.P. & Geraads, D. (2011) New late Pliocene bats (Chiroptera) from Ahl al Oughlam, Morocco. Neues Jahrbuch für Geologie und Palaontologie-Abhandlungen, 260 (1), 55–71.

Hebert, P.D.N., Ratnasingham, S. & de Waard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Philosophical Transactions of the Royal Society of London, B, 270, S596–S599.

Hulva, P., Fornuskova, A., Chudarkova, A., Evin, A., Allegrini, B., Benda, P. & Bryja, J. (2010) Mechanisms of radiation in a bat group from the genus Pipistrellus inferred by phylogeography, demography and population genetics. Molecular Ecology, 19, 5417–5431.

Ibañez, C., Garcia-Mudarra, J.L., Ruedi, M., Stadelmann, B. & Juste, J. (2006) The Iberian contribution to cryptic diversity in European bats. Acta Chiropterologica, 8 (2), 277–297.[277:tictcd];2

Ith, S., Soisook, P., Bumrungsri, S., Kingston, T., Puechmaille, S.J., Struebig, M.J., Bu, S.S.H., Thong, V.D., Furey, N., Hammond, N. & Bates, P.J.J. (2011) A taxonomic review of Rhinolophus coelophyllus Peters 1867 and R. shameli Tate 1943 (Chiroptera: Rhinolophidae) in continental Southeast Asia. Acta Chiropterologica, 13 (1), 41–59.

Jombart, T. (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24 (11), 1403–1405.

Jombart, T., Pontier, D. & Dufour, A.B. (2009) Genetic markers in the playground of multivariate analysis. Heredity, 102 (4), 330–341.

Juste, J., Bilgin, R., Muñoz, J. & Ibañez, C. (2009) Mitochondrial DNA signatures at different spatial scales: from the effects of the Straits of Gibraltar to population structure in the meridional serotine bat (Eptesicus isabellinus). Heredity, 103 (2), 178–187.

Juste, J., Ibañez, C., Muñoz, J., Trujillo, D., Benda, P., Karataş, A. & Ruedi, M. (2004) Mitochondrial phylogeography of the long-eared bats (Plecotus) in the Mediterranean Palearctic and Atlantic Islands. Molecular Phylogenetics and Evolution, 31, 1114–1126.

Kowalski, K. & Rzebik-Kowalska, B. (1991) Mammals of Algeria. Wrocław-Warszawa-Kraków: Ossolineum, 370 pp.

Lack, J.B., Roehrs, Z.P., Stanley, C.E., Ruedi, M. & Van Den Bussche, R.A. (2010) Molecular phylogenetics of Myotis indicate familial-level divergence for the genus Cistugo (Chiroptera). Journal of Mammalogy, 91 (4), 976–922.

Loarie, S.R., Duffy, P.B., Hamilton, H., Asner, G.P., Field, C.B. & Ackerly, D.D. (2009) The velocity of climate change. Nature, 462 (7276), 1052–1055.

Luo, A., Zhang, A., Ho, S., Xu, W., Zhang, Y., Shi, W., Cameron, S. & Zhu, C. (2011) Potential efficacy of mitochondrial genes for animal DNA barcoding: a case study using eutherian mammals. BMC Genomics, 12 (1), 84.

Mayr, E. (1996) What is a species, and what is not? Philosophy of Science, 63 (2), 262–277.

Mein, P. & Tupinier, Y. (1977) Formule dentaire et position systématique du Minioptère (Mammalia, Chiroptera). Mammalia, 41 (2), 207–211.

Miller-Butterworth, C.M., Murphy, W.J., O'Brien, S.J., Jacobs, D.S., Springer, M.S. & Teeling, E.C. (2007) A family matter: conclusive resolution of the taxonomic position of the long-fingered bats, Miniopterus. Molecular Biology and Evolution, 24 (7), 1553–1561.

Monadjem, A., Goodman, S.M., Stanley, W.T. & Appleton, B. (2013) A cryptic new species of Miniopterus from south-eastern Africa based on molecular and morphological characters. Zootaxa, 3746 (1), 123–142.

Monadjem, A., Taylor, P.J., Cotterill, F.P.D. & Schoeman, M.C. (2010) Bats of Southern and Central Africa: A Biogeographic and Taxonomic Synthesis. Johannesburg, South Africa: Wits University Press, 596 pp.

Nicholls, B. & Racey, P.A. (2006a) Contrasting home-range size and spatial partitioning in cryptic and sympatric pipistrelle bats. Behavioral Ecology and Sociobiology, 61 (1), 131–142.

Nicholls, B. & Racey, P.A. (2006b) Habitat selection as a mechanism of resource partitioning in two cryptic bat species Pipistrellus pipistrellus and Pipistrellus pygmaeus. Ecography, 29 (5), 697–708.

Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

Puechmaille, S.J., Allegrini, B., Boston, E., Dubourg-Savage, M.-J., Evin, A., Knochel, A., Le Bris, Y., Lecoq, V., Lemaire, M., Rist, D. & Teeling, E.C. (2012a) Genetic analyses reveal further cryptic lineages within the Myotis nattereri species complex. Mammalian Biology, 77 (3), 224–228.

Puechmaille, S.J., Ar Gouilh, M., Piyapan, P., Yokubol, M., Khin Mie Mie, Bates, P.J.J., Satasook, C., Nwe, T., Bu, S.S.H., Mackie, I.J., Petit, E.J. & Teeling, E.C. (2011) The evolution of sensory divergence in the context of limited gene flow in the bumblebee bat. Nature Communications, 2, 573.

Puechmaille, S.J., Hizem, W.M., Allegrini, B. & Abiadh, A. (2012b) Bat fauna of Tunisia: review of records and new records, morphometrics and echolocation data. Vespertilio, 16, 211–239.

R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (Austria). Available from: (accessed 10 February 2014)

Reeder, D.M., Helgen, K.M. & Wilson, E.O. (2007) Global trends and biases in new mammal species discoveries. Occasional Papers, Museum of Texas Tech University, 269, 1–35.

Rice, W.R. (1989) Analyzing tables of statistical tests. Evolution, 43 (1), 223–225.

Rousset, F. (2008) genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Notes, 8, 103–106.

Salicini, I., Ibañez, C. & Juste, J. (2011) Multilocus phylogeny and species delimitation within the Natterer’s bat species complex in the Western Palearctic. Molecular Phylogenetics and Evolution, 61, 888–898.

Simmons, N.B. (2005) Order Chiroptera. In: Wilson, D.E. & Reeder, D.M. (Eds), Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore, pp. 312–529.

Smith, M.F. & Patton, J.L. (1993) The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biological Journal of the Linnean Society, 50, 149–177.

Šrámek, J., Gvoždík, V. & Benda, P. (2013) Hidden diversity in bent-winged bats (Chiroptera: Miniopteridae) of the Western Palaearctic and adjacent regions: implications for taxonomy. Zoological Journal of the Linnean Society, 167 (1), 165–190.

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28 (10), 2731–2739.

Thong, V.D., Puechmaille, S.J., Denzinger, A., Bates, P.J.J., Dietz, C., Csorba, G., Soisook, P., Teeling, E.C., Matsumura, S., Furey, N. & Schnitzler, H.U. (2012a) Systematics of the Hipposideros turpis complex and a description of a new subspecies from Vietnam. Mammal Review, 42 (2), 166–192.

Thong, V.D., Puechmaille, S.J., Denzinger, A., Csorba, G., Dietz, C., Bates, P.J.J., Teeling, E.C. & Schnitzler, H.-U. (2012b) A new species of Hipposideros (Chiroptera: Hipposideridae) from Vietnam. Journal of Mammalogy, 93 (1), 1–11.

Walters, C.L., Freeman, R., Collen, A., Dietz, C., Fenton, M.B., Jones, G., Obrist, M.K., Puechmaille, S.J., Sattler, T., Siemers, B.M., Jones, K.E. & Parsons, S. (2012) A continental-scale tool for acoustic identification of European bats. Journal of Applied Ecology, 49, 1064–1074.

Wilkinson, G.S. & Chapman, A.M. (1991) Length and sequence variation in evening bat D-Loop mtDNA. Genetics, 128, 607–617.

Yoshiyuki, M. (1989) A systematic study of the Japanese Chiroptera. National Science Museum monographs, 7, 1–242.


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