ArticlePDF Available

Description of a new species of the Miniopterus aelleni group (Chiroptera: Miniopteridae) from upland areas of central and northern Madagascar

Authors:
Steven Michael Goodman at Field Museum of Natural History
Steven Michael Goodman
Beza Ramasindrazana at University of Antananarivo
Beza Ramasindrazana
Kate Marilyn Naughton at Museum Victoria
Kate Marilyn Naughton
Belinda Appleton
Belinda Appleton
Belinda Appleton
  • This person is not on ResearchGate, or hasn't claimed this research yet.
Download full-text PDF
Read full-text
Download citation

Abstract

Recent molecular genetic work, combined with morphological comparisons, on Malagasy members of the bat genus Miniopterus (Family Miniopteridae), has uncovered a number of cryptic species. Based on recently collected specimens and associated tissues, we examine patterns of variation in M. aelleni, the holotype of which comes from Ankarana in northern Madagascar. Using molecular genetic (mitochondrial cytochrome b) and morphological characters we describe a new species, M. ambohitrensis sp. nov. In northern Madagascar, M. ambohitrensis and M. aelleni are allopatric, but occur in relatively close geographical contact (approximately 40 km direct line distance) with M. ambohitrensis found at Montagne d'Ambre in montane humid forest and M. aelleni sensu stricto at Ankarana in dry deciduous forest. Morphologically, this new taxon is differentiated from M. aelleni based on pelage coloration, external measurements, craniodental differences, and tragus shape. Comparisons using 725 bp of cytochrome b found a divergence of 1.1% within M. aelleni sensu stricto, 0.8% within M. ambohitrensis, and 3.3% between these two clades. The two sister species do not demonstrate acoustical differences based on recordings made in a flight cage. Miniopterus ambohitrensis is known from four localities in the northern and central portions of Madagascar, all from montane regions and across an elevational range from about 800 to 1600 m; its calculated "Extent of occurrence" is 15,143 km2. It is possible that this species is at least partially migratory.
Content uploaded by Beza Ramasindrazana
Author content
All content in this area was uploaded by Beza Ramasindrazana on May 01, 2015
Content may be subject to copyright.
538
Accepted by P. Velazco: 17 Feb. 2015; published: 23 Mar. 2015
ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN
1175-5334
(online edition)
Copyright © 2015 Magnolia Press
Zootaxa 3936 (4): 538
–
558
www.mapress.com
/
zootaxa
/
Article
http://dx.doi.org/10.11646/zootaxa.3936.4.4
http://zoobank.org/urn:lsid:zoobank.org:pub:26655EB2-0352-4D4F-BBD6-44F89D05DC41
Description of a new species of the Miniopterus aelleni group (Chiroptera:
Miniopteridae) from upland areas of central and northern Madagascar
STEVEN M. GOODMAN
1,2,9
, BEZA RAMASINDRAZANA
2,3,4,5
,
KATE M. NAUGHTON
6
& BELINDA APPLETON
7,8
1
Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, Illinois 60605, USA. E-mail: sgoodman@fieldmuseum.org
2
Association Vahatra, BP 3972, Antananarivo (101), Madagascar. E-mails: sgoodman@vahatra.mg, ramasindrazana@gmail.com
3
Département de Biologie Animale, Faculté des Sciences, Université d’Antananarivo, BP 906, Antananarivo (101), Madagascar
4
Centre de Recherche et de Veille sur les maladies émergentes dans l’Océan Indien, 2 rue Maxime Rivière, 97490 Sainte Clotilde, La
Réunion, France
5
Institut de Recherche pour le Développement, 97492 Sainte Clotilde, La Réunion, France
6
Marine Invertebrates, Sciences Department, Museum Victoria, GPO Box 666, Melbourne 3001, Victoria, Australia.
E-mail: kmnaughton@gmail.com
7
Department of Genetics, University of Melbourne, Victoria 3010, Australia. E-mail: b.appleton@unimelb.edu.au
8
Life and Environmental Science, Deakin University, Victoria, 3216, Australia. E-mail: belinda.appleton@deakin.edu.au
9
Corresponding author
Abstract
Recent molecular genetic work, combined with morphological comparisons, on Malagasy members of the bat genus Min-
iopterus (Family Miniopteridae), has uncovered a number of cryptic species. Based on recently collected specimens and
associated tissues, we examine patterns of variation in M. aelleni, the holotype of which comes from Ankarana in northern
Madagascar. Using molecular genetic (mitochondrial cytochrome b) and morphological characters we describe a new spe-
cies, M. ambohitrensis sp. nov. In northern Madagascar, M. ambohitrensis and M. aelleni are allopatric, but occur in rel-
atively close geographical contact (approximately 40 km direct line distance) with M. ambohitrensis found at Montagne
d’Ambre in montane humid forest and M. aelleni sensu stricto at Ankarana in dry deciduous forest. Morphologically, this
new taxon is differentiated from M. aelleni based on pelage coloration, external measurements, craniodental differences,
and tragus shape. Comparisons using 725 bp of cytochrome b found a divergence of 1.1% within M. aelleni sensu stricto,
0.8% within M. ambohitrensis, and 3.3% between these two clades. The two sister species do not demonstrate acoustical
differences based on recordings made in a flight cage. Miniopterus ambohitrensis is known from four localities in the
northern and central portions of Madagascar, all from montane regions and across an elevational range from about 800 to
1600 m; its calculated “Extent of occurrence” is 15,143 km
2
. It is possible that this species is at least partially migratory.
Key words: taxonomy, morphology, molecular genetics, new species, montane, humid formation forest, cryptic species
Résumé
Les études morphologiques et moléculaires récemment entreprises sur les espèces du genre Miniopterus (Famille des Min-
iopteridae) ont révélé la présence de diverses espèces cryptiques. Dans la présente étude, nous avons analysé des spéci-
mens récemment collectés et les tissus associés afin de déterminer la variation de M. aelleni dont l’holotype vient du Parc
National d’Ankarana, situé dans la partie Nord de Madagascar. En se basant sur les données moléculaires (cytochrome b)
et morphologiques, nous avons décrit une nouvelle espèce, M. ambohitrensis sp. nov. Dans la partie nord malgache, M.
aelleni et M. ambohitrensis vivent en allopatrie. Ces deux espèces sont réparties dans des zones géographiquement
proches (distantes d’environ 40 km à vol d’oiseau) avec M. ambohitrensis dans des zones de forêts humides de montagne
du Parc National de la Montagne d’Ambre et M. aelleni sensu stricto, dans des zones dominées par des forêts sèches ca-
ducifoliées du Parc National d’Ankarana. Du point de vue morphologique, cette nouvelle espèce de Miniopterus se dis-
tingue de M. aelleni par la couleur du pelage, les mensurations externes et cranio-dentaires ainsi que la forme du tragus.
L’analyse des 725 pb du cytochrome b montre une divergence génétique de 1,1 % chez M. aelleni sensu stricto et de 0,8
Zootaxa 3936 (4) © 2015 Magnolia Press
·
555
NEW SPECIES OF MINIOPTERUS BAT FROM MADAGASCAR
months (June through August) ranged from 9.7 to 11.2°C (Langrand 1995). We have found bats at the site in torpor,
but no evidence of deep hibernation.
In a more practical sense, the species described herein, M. ambohitrensis, can be separated from its sister
species, M. aelleni, by a number of morphological characters, including size, coloration, tragus shape, and
craniodental features. These two species have allopatric distributions. As has been shown for several genetically
distinct cryptic species of small to moderate size Malagasy Miniopterus, tragus shape can be diagnostic to
distinguish taxa and can be used to diagnose different clades (Goodman et al. 2007, 2008, 2009a, 2009b, 2010,
2011). Miniopterus ambohitrensis possesses a number of mensural and phenotypic characters, including tragus
shape, which allows it to be distinguished from M. aelleni. A detailed study overlaying clade allocation with a
variety of different genetic markers and morphological variation, specifically tragus shape, as well as bioacoustic
characteristics is needed to resolve the affinities of animals currently placed in the P-group.
Acknowledgements
Conservation International (CABS), The John T. and Catherine D. MacArthur Foundation, and the Volkswagen
Foundation have generously supported field research associated with this paper. We are grateful to the Direction du
Système des Aires Protégées, Direction Générale de l’Environnement et des Forêts, and Madagascar National
Parks (ex. Association National pour la Gestion des Aires Protégées or ANGAP) for issuing permits to conduct
faunal surveys and aid in numerous ways. Yann Gomard, Corrie M. Schoeman, and Peter Taylor helped with
fieldwork. For access to specimens under their care, we are indebted to Kristofer Helgen, USNM; Jean-Marc Pons,
MNHN; and Daniel Rakotondravony, UADBA. Herivololona Mbola Rakotondratsimba kindly prepared Figure 1
and John Weinstein Figures 4 and 5. BR received a postdoctoral fellowship from the RunEmerge project funded by
the European Frame work program FP7 Capacities/Regpot, and post-doctoral grants from Fonds de Coopération
Régionale of the Préfecture de La Réunion and from the Dr. Ralph and Marian Falk Medical Research Trust to The
Field Museum of Natural History, Chicago. We would like to thank an anonymous reviewer for their detailed
comments on an earlier version of the ms.
References
Appleton, B.R., McKenzie, J.A. & Christidis, L. (2004) Molecular systematics and biogeography of the bent-wing bat complex
Miniopterus schreibersii (Kuhl, 1817) (Chiroptera: Vespertilionidae). Molecular Phylogenetics and Evolution, 31,
431–439.
http://dx.doi.org/10.1016/j.ympev.2003.08.017
Battistini, R. (1965) Problèmes géomorphologiques de l’Extrême Nord de Madagascar. Madagascar, Revue de Géographie, 7,
1–61.
Bernard, R.T.F. (1980) Reproductive cycles of Miniopterus schreibersi natalensis (Kuhl, 1819) and M. fraterculus Thomas and
Schwann, 1906. Annals of the Transvaal Museum, 32, 55–64.
Bilgin, R., Gürün, K., Maraci, O., 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, 279–289.
http://dx.doi.org/10.3161/150811012X661611
Brenon, P. (1972) The geology of Madagascar. In: Battistini, R. & Richard-Vindard, G. (Eds.), Biogeography and ecology in
Madagascar. Dr. W. Junk, The Hague, pp. 27–86.
Cardinal, B.R. & Christidis, L. (2000) Mitochondrial DNA and morphology reveal three geographically distinct lineages of the
large bentwing bat (Miniopterus schreibersii) in Australia. Australian Journal of Zoology, 48, 1–19.
http://dx.doi.org/10.1071/ZO99067
Christidis, L., Goodman, S.M., Naughton, K. & Appleton, B. (2014) Insights into the evolution of a cryptic radiation of bats:
dispersal and ecological radiation of Malagasy Miniopterus (Chiroptera: Miniopteridae). PLoS ONE, 9 (3), e92440.
http://dx.doi.org/10.1371/journal.pone.0092440
Donque, G. (1975) Contribution à l’étude du climat de Madagascar. Nouvelle Imprimerie des Arts Graphiques, Antananarivo,
478 pp.
Furman, A., Oztunc, T. & Coraman, 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, 61–72.
GOODMAN ET AL.
556
·
Zootaxa 3936 (4) © 2015 Magnolia Press
http://dx.doi.org/10.3161/150811010X504581
Gemmel, N.J. & Akiyama, S. (1996) An efficient method for the extraction of DNA from vertebrate tissues. Trends in Genetics,
12, 338–339.
http://dx.doi.org/10.1016/S0168-9525(96)80005-9
Goodman, S.M. (2011) Les chauves-souris de Madagascar. Association Vahatra, Antananarivo, 129 pp.
Goodman, S.M. & Ramasindrazana, B. (2013) Bats or the Order Chiroptera. In: Goodman, S.M. & Raherilalao, M.J. (Eds.),
Atlas of selected land vertebrates of Madagascar. Association Vahatra, Antananarivo, pp. 169–209.
Goodman, S.M., Ryan, K.E., Maminirina, C.P., Fahr, J., Christidis, L. & Appleton, B. (2007) The specific status of populations
on Madagascar referred to Miniopterus fraterculus (Chiroptera: Vespertilionidae), with description of a new species.
Journal of Mammalogy, 88, 1216–1229.
http://dx.doi.org/10.1644/06-MAMM-A-285R1.1
Goodman, S.M., Bradman, H.M., Maminirina, C.P., Ryan, K.E., Christidis, L. & Appleton, B. (2008) A new species of
Miniopterus (Chiroptera: Miniopteridae) from lowland southeastern Madagascar. Mammal Biology, 73, 199–213.
http://dx.doi.org/10.1016/j.mambio.2007.12.003
Goodman, S.M., Maminirina, C.P., Weyeneth, N., Bradman, H.M., Christidis, L., Ruedi, M. & Appleton, B. (2009a) 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, 339–363.
http://dx.doi.org/10.1111/j.1463-6409.2008.00377.x
Goodman, S.M., Maminirina, C.P., Bradman, H.M., Christidis, L. & Appleton, B. (2009b) The use of molecular phylogenetic
and morphological tools to identify cryptic and paraphyletic species: examples from the diminutive long-fingered bats
(Miniopterus: Miniopteridae: Chiroptera) on Madagascar. American Museum Novitates, 3669, 1–33.
Goodman, S.M., Maminirina, C.P., Bradman, H.M., Christidis, L. & Appleton, B. (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, 75–86.
http://dx.doi.org/10.1111/j.1439-0469.2009.00524.x
Goodman, S.M., Ramasindrazana, B., Maminirina, C.P., Schoeman, M.C. & Appleton, B. (2011) Morphological, bioacoustical,
and genetic variation in Miniopterus bats from eastern Madagascar, with the description of a new species. Zootaxa, 2880,
1–19.
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum
likelihood. Systematic Biology, 52, 696–704.
http://dx.doi.org/10.1080/10635150390235520
Harper, G.J., Steininger, M.K., Tucker, C.J., Juhn, D. & Hawkins, F. (2007) Fifty years of deforestation and forest
fragmentation in Madagascar. Environmental Conservation, 34, 325–333.
http://dx.doi.org/10.1017/S0376892907004262
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.
http://dx.doi.org/10.1093/bioinformatics/17.8.754
Hurlbert, S.H. (1984) Pseudoreplication and the design of ecological field experiments. Ecological Monographs, 54, 187–211.
http://dx.doi.org/10.2307/1942661
Irwin, D.M., Kocher, T.D. & Wilson, A.C. (1991) Evolution of the cytochrome b gene of mammals. Journal of Molecular
Evolution, 32, 128–144.
http://dx.doi.org/10.1007/BF02515385
IUCN (2012) IUCN Red List categories and criteria: version 3.1. Second Edition. International Union for the Conservation of
Nature, Gland, Switzerland and Cambridge, 32 pp.
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of
nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.
http://dx.doi.org/10.1007/BF01731581
Koopman, K.F. (1994) Chiroptera: Systematics. In: Niethammer, J., Schliemann, H. & Starck, D. (Eds) Handbook of Zoology.
Vol. 8. Walter de Gruyter, Berlin, pp. 1–217.
Langrand, O. (1995) The effects of forest fragmentation on bird species in Madagascar: A case study from Ambohitantely
Forest Reserve on the Central High Plateau. Master of Science, Department of Zoology and Entomology, University of
Natal, Pitermaritzburg. [total page number unkown]
Miller-Butterworth, C.M., Eick, G., Jacobs, D.S., Schoeman, M.C. & Harley, E.H. (2005) Genetic and phenotypic differences
between South African long-fingered bats, with a global miniopterine phylogeny. Journal of Mammalogy, 86, 1121–1135.
http://dx.doi.org/10.1644/05-MAMM-A-021R1.1
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.
http://dx.doi.org/10.11646/zootaxa.3746.1.5
Obrist, M.K. (1995) The influence of individual, habitat and conspecifics on sonar signal design. Behavioral Ecology and
Sociobiology, 36, 207–219.
http://dx.doi.org/10.1007/BF00177798
Onyango, D.W., Gachoka, J.M., Otiang’a-Owiti, G.E. & Hendrickx, A.G. (1995) Seasonally dependent testicular apoptosis in
Zootaxa 3936 (4) © 2015 Magnolia Press
·
557
NEW SPECIES OF MINIOPTERUS BAT FROM MADAGASCAR
the tropical long-fingered bat (Miniopterus inflatus). Zeitschrift für Säugetierkunde, 60, 206–214.
Peterson, R.L., Eger, J.L. & Mitchell, L. (1995) Chiroptères. Vol. 84. Faune de Madagascar. Muséum national d’Histoire
naturelle, Paris, 204 pp.
Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256.
http://dx.doi.org/10.1093/molbev/msn083
Puechmaille, S.J., Allegrini, B., Benda, P., Gürün, K., Šrámek, J., Ibañez, C., Juste, J. & Bilgin, R. (2014) A new species of the
Miniopterus schreibersii species complex (Chiroptera: Miniopteridae) from the Maghreb Region, North Africa. Zootaxa,
3794 (1), 108–124.
http://dx.doi.org/10.11646/zootaxa.3794.1.4
Rabearivony, J., Thorstrom, R., Rene de Roland, L.-A., Rakotondratsima, M., Andriamalala, T.R.A., Sam, T.S., Razafimanjato,
G., Rakotondravony, D., Raselimanana, A.P. & Rakotoson, M. (2010) Protected area surface extension in Madagascar: Do
endemism and threatened species remain useful criteria for site selection? Madagascar Conservation and Development, 5,
35–47.
Ramasindrazana, B. & Goodman, S.M. (2014) Documented record of Triaenops menamena (Family Hipposideridae) in the
Central Highlands of Madagascar. African Bat Conservation News, 35, 6–7.
Ramasindrazana, B., Goodman, S.M., Schoeman, M.C. & Appleton, B. (2011) Identification of cryptic species of Miniopterus
bats (Chiroptera: Miniopteridae) from Madagascar and the Comoros using bioacoustics overlaid on molecular genetic and
morphological characters. Biological Journal of the Linnean Society, 104, 284–302.
http://dx.doi.org/10.1111/j.1095-8312.2011.01740.x
R Core Team. (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing,
Vienna. Available from: http://www.R-project.org/ (accessed 18 February 2015)
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liang, L., Suchard, M.A. &
Huelsenbeck, J.P. (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model
space. Systematic Biology, 61, 539–542.
http://dx.doi.org/10.1093/sysbio/sys029
Rossi, G. (1974) Review of J.P. Karche. 1972. Contribution à l’étude géologique de la Montagne d’Ambre et des régions
voisines du Nord de Madagascar. Thèse d’Etat (Sciences), Université de Besançon. Madagascar. Revue de Géographie, 24,
95–96.
Schatz, G. (2000) Endemism in the Malagasy flora. In: Lourenço, W.R. & Goodman, S.M. (Eds.), Diversité et endémisme à
Madagascar. Mémoires de la Société de Biogéographie, Paris, pp. 1–8.
Schnitzler, H.-U. & Kalko, E.K.V. (2001) Echolocation by insect-eating bats. Bioscience, 51, 557–569.
http://dx.doi.org/10.1641/0006-3568(2001)051[0557:EBIEB]2.0.CO;2
Schoeman, M.C. & Jacobs, D.S. (2008) The relative influence of competition and prey defenses on the phenotypic structure of
insectivorous bat ensembles in southern Africa. PLoS ONE, 3 (11), e3715.
http://dx.doi.org/10.1371/journal.pone.0003715
Schoeman, M.C., Goodman, S.M., Ramasindrazana, B. & Kabinouva, D. (2015) Species interactions during diversification and
community assembly in Malagasy Miniopterus bats. Evolutionary Ecology, 29, 17–47.
http://dx.doi.org/10.1007/s10682-014-9745-4
Siemers, B.M. (2004) Bats in the field and in a flight cage: recording and analysis of their echolocation calls and behavior. In:
Brigham, R.M., Kalko, E.K.V., Jones, G., Parsons, S. & Limpens, H.J.G.A. (Eds.), Bat echolocation research: tools,
techniques and analysis. Bat Conservation International, Austin, Texas, pp. 107–113.
Smith, M.F. & Patton, J.L. (1991) Variation in mitochondrial cytochrome b sequence in natural populations of South American
akodontine rodents (Muridae: Sigmodontinae). Molecular Biology and Evolution, 8, 85–103.
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, 165–190.
http://dx.doi.org/10.1111/j.1096-3642.2012.00870.x
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, 2371–2739.
http://dx.doi.org/10.1093/molbev/msr121
Toews, D.P.L. & Brelsford, A. (2012) The biogeography of mitochondrial and nuclear discordance in animals. Molecular
Ecology, 21 (16), 3907–3930.
http://dx.doi.org/10.1111/j.1365-294X.2012.05664.x
van der Merwe, M. (1975) Preliminary study on the annual movements of the Natal clinging bat. South African Journal of
Science, 71, 237–241.
van der Merwe, M. (1979) Growth of ovarian follicles in the Natal clinging bat. South African Journal of Science, 14, 111–117.
Voigt, C.C., Helbig-Bonitz, M., Kramer-Schadt, S. & Kalko, E.K.V. (2014) The third dimension of bat migration: Evidence for
elevational movements of Miniopterus natalensis along the slopes of Mount Kilimanjaro. Oecologia, 174, 751–764.
http://dx.doi.org/10.1007/s00442-013-2819-0
Zwickl, D.J. (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under
the maximum likelihood criterion. PhD thesis, University of Texas, Austin.
... Besides the genus Murina (which increased from 17 to 40 species since 2005 - Burgin et al., 2020), no other speciose bat genus has seen such a proportionate increase in numbers of species over this period, underscoring the cryptic nature of speciation in the genus Miniopterus (Goodman et al., 2009a(Goodman et al., , 2009b. Genetic surveys have greatly aided the discovery of cryptic species in Miniopterus, especially among Afrotropical and Malagasy forms (Juste et al., 2007;Goodman et al., 2009bGoodman et al., , 2011Goodman et al., , 2015Furman et al., 2010;Puechmaille et al., 2014;Monadjem et al., 2019Monadjem et al., , 2020Demos et al., 2020). However, less attention has been paid to Asian forms, and for a long time, many larger Miniopterus from this continent were recognized as various subspecies of M. schreibersii (Simmons, 2005). ...
... Mitochondrial markers have been widely used in other studies on Miniopterus spp. (Goodman et al., 2008(Goodman et al., , 2009a(Goodman et al., , 2010(Goodman et al., , 2015Puech maille et al., 2014;Monadjem et al., 2019Monadjem et al., , 2020. The new species has been described based on substantial mitochondrial DNA divergence (8.46-9.27%) ...
... The level of mitochondrial DNA divergence equals or exceeds those in other published studies on Miniopterus species (Goodman et al., 2008(Goodman et al., , 2009a(Goodman et al., , 2010Puechmaille et al., 2014). For instance, these genetic distances considerably exceed mitochondrial DNA divergence between M. wilsoni and M. minor (4.1-5.7%) in Monadjem et al. (2020) or the 3.3% divergence between M. ambohitrensis and M. aelleni in Goodman et al. (2015). Strikingly, the various Malagasy species of Miniopterus studied by Goodman and collaborators were reexamined using five nuclear intron sequences, and in each case their distinction as valid species was maintained (Demos et al., 2020). ...
DNA Barcoding and Morphological Analyses Reveal a Cryptic Species of Miniopterus from India and Sri Lanka
Article
  • Jul 2022
  • ACTA CHIROPTEROL
The genus Miniopterus is a monophyletic assemblage of many species characterized by remarkably conservative morphology. The number of recognized species has more than doubled over the last two decades, mainly with newly recognized Afrotropical and Malagasy species. A molecular phylogenetic analysis based on cytochrome c oxidase subunit I (COI) revealed a monophyletic clade of Miniopterus from Sri Lanka and southern India that is distinct from the other known taxa of this genus. The mean uncorrected pairwise sequence divergence among the three gene sequences of this new Miniopterus lineage was 0.83% (range 0.4–1.2%) and between this and other sampled taxa was 12.7% (range 8.5–15.9%). This lineage was also distinctive in craniodental morphometrics and hence it is herein described as a new species. The newly described species is easily distinguished by its external and cranial dimensions from its smaller (M. pusillus) and larger (M. magnater) congeners in India and Sri Lanka. It is also somewhat smaller than M. fuliginosus in both external and cranial dimensions. This is the first description of a new Miniopterus species from Asia in six decades and from India and Sri Lanka in eight decades. Our study highlights the importance of using both genetic and morphometric analyses in taxonomic studies on South Asian bats. Key words: cryptic species, Miniopteridae, cytochrome oxidase 1, morphometrics, taxonomy, South Asia, DNA barcode
View
... Sixty-nine Zootaxa studies described 76 new living mammals (see Appendix I), including Niviventer pianmaensis, which was described as a subspecies (Li & Yang 2009), and Conilurus capricornensis, which was described from cave material but is thought to still be extant (Cramb & Hocknull 2010). The vast majority of studies ( Figure 5) employed an integrative approach, with a combination of two or more types of data, including detailed comparative anatomy analyses, especially of cranial, dental, and integumental anatomy, but also bacular (e.g., Kruskop et al. 2019); morphometric multivariate analyses, based mainly on craniometric traditional measurements using principal component and discriminant analyses, but also employing MANOVA (Goodman et al. 2015) or using a geometric morphometrics approach (Cucchi et al. 2006;Taylor et al. 2011); phylogenetic analyses of molecular sequence data, especially cytochrome b, but also cytochrome oxidase 1, d-loop, ribosomal 12s and 15s, ND2, and nuclear loci such as IRBP and RAG1; classic cytogenetics, especially for rodents but also used in the description of the vespertilionid bat Laephotis stanleyi ; and comparative echolocation analyses for bats (e.g., Reardon et al. 2008;Soisook et al. 2013Soisook et al. , 2015Soisook et al. , 2017Goodman et al. 2011Goodman et al. , 2015Puechmaille et al. 2014). Other sources of data less commonly employed in species descriptions were allozymes (Reardon et al. 2008;Verheyen et al. 2011), microsatellites Ralph et al. 2015), and niche modeling (Ralph et al. 2015). ...
... Sixty-nine Zootaxa studies described 76 new living mammals (see Appendix I), including Niviventer pianmaensis, which was described as a subspecies (Li & Yang 2009), and Conilurus capricornensis, which was described from cave material but is thought to still be extant (Cramb & Hocknull 2010). The vast majority of studies ( Figure 5) employed an integrative approach, with a combination of two or more types of data, including detailed comparative anatomy analyses, especially of cranial, dental, and integumental anatomy, but also bacular (e.g., Kruskop et al. 2019); morphometric multivariate analyses, based mainly on craniometric traditional measurements using principal component and discriminant analyses, but also employing MANOVA (Goodman et al. 2015) or using a geometric morphometrics approach (Cucchi et al. 2006;Taylor et al. 2011); phylogenetic analyses of molecular sequence data, especially cytochrome b, but also cytochrome oxidase 1, d-loop, ribosomal 12s and 15s, ND2, and nuclear loci such as IRBP and RAG1; classic cytogenetics, especially for rodents but also used in the description of the vespertilionid bat Laephotis stanleyi ; and comparative echolocation analyses for bats (e.g., Reardon et al. 2008;Soisook et al. 2013Soisook et al. , 2015Soisook et al. , 2017Goodman et al. 2011Goodman et al. , 2015Puechmaille et al. 2014). Other sources of data less commonly employed in species descriptions were allozymes (Reardon et al. 2008;Verheyen et al. 2011), microsatellites Ralph et al. 2015), and niche modeling (Ralph et al. 2015). ...
The role and impact of Zootaxa in mammalogy in its first 20 years
Article
  • May 2021
Zootaxa came as a new and innovative publication medium for taxonomy, amidst a scenario of devaluation of this important biological science. After 20 years, it has ascertained itself as one of the main journals in animal taxonomy. However, the contribution of the journal to the taxonomy of Mammalia (mammals), one of the most studied groups of animals with a long-standing, dedicated spectrum of specialized journals (mammalogy), could have been expected as minor. All the current and former editors of the Mammalia section of Zootaxa analyzed the relative contribution of the journal to the description of new species of mammals since 2001. We also analyzed the contribution of Zootaxa by taxon, geographic origin of taxa, and geographic origin of first authors. The taxonomic methodology of authors in species description is described as well as the temporal trends in publications and publication subjects. We highlight the editors’ picks and eventually, the challenges for the future. We found that Zootaxa has had a significant contribution to mammalogy, being the second journal (the first being Journal of Mammalogy) in terms of number of new species described (76; 10.6% of the new mammalian species described between 2001 and 2020). The majority of the new species were described following an integrative taxonomic approach with at least two sources of data (86%). The analysis of published taxa, their geographic origin, and the country of origin of first authors shows a wide coverage and exhaustive representation, except for the species from the Nearctic. We conclude that Zootaxa has likely responded to a repressed demand for an additional taxonomic journal in mammalogy, with as possible appeals the absence of publication fees and an established publication speed. With 246 articles published in the past 20 years, the Mammalia section of Zootaxa embraces a large spectrum of systematic subjects going beyond alpha taxonomy. The challenges for the future are to encourage publications of authors from the African continent, still poorly represented, and from the palaeontology community, as the journal has been open to palaeontology since its early days.
View
... The genus Miniopterus appears to be particularly rich in cryptic species, clearly demonstrated by the rapid increase in the number of recognized species since the application of molecular techniques to systematic studies of this group (Goodman et al., 2007(Goodman et al., , 2009. In 2005, just four species of Miniopterus were recognized on Madagascar (Simmons, 2005); within 10 years that number had risen to 12 species (Christidis et al., 2014;Goodman et al., 2015). ...
... In this paper, we present new information on a population of Miniopterus from Mozambique showing that it represents a new species to science. This is the second new Miniopterus species to be described from this country in the past decade and follows a trend of new discoveries in Madagascar and West Africa (Christidis et al., 2014;Goodman et al., 2015;Monadjem et al., 2019). Considering the recent phylogeny for Miniopterus by Demos et al. (2019), it would appear that these new species descriptions are just the tip of the iceberg, as predicted by Monadjem et al. (2013a). ...
View
... Since there are various categories of endemism and no universally recognized method to measure endemism levels [47], the number of microendemics and regional endemics among terrestrial Malagasy mammal species may be even higher, depending on the concept applied. The discovery of many cryptic Microcebus species over the past decades [13], along with recent molecular studies of the bat genera Hipposideros [48] and Miniopterus [49], further suggest an increasing number of terrestrial Malagasy mammal species. Given the heightened risk of extinction for undiscovered mammal species [31], the continuous deforestation in Madagascar [23], and the vast area of endemism centers throughout the country [34], on-site conservation should be one of the substantial pillars of conserving terrestrial mammal species in Madagascar. ...
Prioritising Ex Situ Conservation for Malagasy Mammal Species in Line with IUCN's 'One Plan Approach to Conservation'
Article
Full-text available
Madagascar, as one of the global biodiversity hotspots, hosts numerous unique terrestrial mammal species that need urgent protection. To identify priority species for conservation, an updated list of terrestrial Malagasy mammal species was compiled, including their threat status, distribution, endemism level, Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) listing, and Evolutionarily Distinct and Globally Endangered (EDGE) score. An overview of these species kept in zoos worldwide was created using the Zoological Information Management System and Zootierliste to assess ex situ conservation efforts. Nearly 60% of the 212 native terrestrial mammal species are threatened with extinction, with 18% being regional endemics, 39% microendemics, and 42% endemics. The majority of these species (92%) occur within protected areas. About half of Madagascar's mammals are listed under CITES, and less than half have an EDGE score. Only 34 species are kept in zoos globally, with 26 Red-Listed as threatened. Nine out of seventeen families are not represented in zoos. A total of 1545 institutions, primarily in Europe and North America, keep Malagasy mammal species, with successful reproduction reported for 28 species in the last 12 months, 23 of them listed as threatened on the IUCN Red List. To maximize conservation, we recommend reallocating resources towards priority species and implementing concerted ex situ and in situ actions as proposed by the IUCN's One Plan Approach.
View
... The phenotypes of cryptic species do not differ much because of the evolutionary convergence that comes from having similar lifestyles. Cryptic species have been described in mammals, including bats (Barratt et al., 1997;Goodman and Ramasindrazana, 2015;López-Wilchis et al., 2016;Soisook et al., 2016;Juste et al., 2019;Srinivasulu et al., 2019), pikas (Koju et al., 2017), rodents (Riddle et al., 2014;Hulme-Beaman et al., 2018), and primates (Hotaling et al., 2016). A recent study detected cryptic divergence in the snowshoe hare (Lepus americanus) (Melo-Ferreira et al., 2014b). ...
Evolutionary ecology of hares (Lepus spp.) from northwestern Africa; The problem of cryptic species and the description of a new species (Lepus saharae sp. nov.)
Article
Full-text available
  • Jun 2020
  • EVOL ECOL RES
https://www.evolutionary-ecology.com/issues/forthcoming/ar3207.pdf Objective: We examine the different pressures that lead to the occurrence of new species and thus to their phylogenies. From the point of view of evolutionary ecology, we seek to examine — in addition to the phylogenetic relationships of different lineages — the evolutionary pressures that lead to them and, in some cases, mask them. Organisms and locales: We study hares (Lepus spp.) in northwestern Africa. These hares are morphologically similar, making it appear superficially that there is only one species. Methods: We describe different populations of hares in northwestern Africa. We describe the morphology of the new species and furnish photographs of specimens from across the study area. We analyse five mitochondrial DNA fragments. Results: The mitochondrial DNA analysis revealed the presence of three Lepus species. They are different from both Lepus capensis and Lepus victoriae and have contiguous, partially overlapping geographical distribution. One of the species, present in the western Sahara (Morocco), is new (Lepus saharae sp. nov.). The other two species (Lepus mediterraneus Wagner, 1841 and Lepus schlumbergeri Saint-Loup, 1894) live in northern and central parts of Morocco, and have already been described above. The distribution of at least two of the three species extends to other countries. Various ecoevolutionary pressures have caused this diversity to go unnoticed before now. Surely the species need to adapt to different environments such as mountain or desert; and isolation of their populations by distance, by climatic or geographical barriers will also cause – or at least allow — them to appear different. Yet some evolutionary pressures have made them converge morphologically, making it appear that there is only one species
View
A new species of the Miniopterus australis species complex (Chiroptera: Miniopteridae) from the Western Ghats, India
Article
  • May 2023
The genus Miniopterus is highly diverse in cryptic species. Based on integrated approaches of morphometrics, echolocation call analysis, and molecular phylogenetics, we present evidence of a hitherto undescribed species, Srini’s Bent-winged bat Miniopterus srinii sp. nov.. The new species, found in the Western Ghats of southern Karnataka, India, closely resembles the Small Bent-winged bat Miniopterus pusillus, found elsewhere in Karnataka, Kerala, and Tamil Nadu, India. Although it shows external similarity with Miniopterus pusillus sensu stricto from the Nicobar Islands, the new species is relatively larger and distinct in craniodental measurements and echolocation call parameters, despite slight overlaps. Importantly, Miniopterus srinii exhibits morphological convergence with Miniopterus pusillus as despite similarities in morphologies, there is a significant genetic distance of 10.84 ± 0.22%. The new cryptic species shares distribution with Miniopterus phillipsi and Miniopterus pusillus in the Western Ghats, further highlighting the need to study both the genus’ cryptic diversity, and the region’s conservation importance.
View
View
View
Bat coronavirus phylogeography in the Western Indian Ocean
Article
Full-text available
  • Dec 2020
Bats provide key ecosystem services such as crop pest regulation, pollination, seed dispersal, and soil fertilization. Bats are also major hosts for biological agents responsible for zoonoses, such as coronaviruses (CoVs). The islands of the Western Indian Ocean are identified as a major biodiversity hotspot, with more than 50 bat species. In this study, we tested 1,013 bats belonging to 36 species from Mozambique, Madagascar, Mauritius, Mayotte, Reunion Island and Seychelles, based on molecular screening and partial sequencing of the RNA-dependent RNA polymerase gene. In total, 88 bats (8.7%) tested positive for coronaviruses, with higher prevalence in Mozambican bats (20.5% ± 4.9%) as compared to those sampled on islands (4.5% ± 1.5%). Phylogenetic analyses revealed a large diversity of α- and β-CoVs and a strong signal of co-evolution between CoVs and their bat host species, with limited evidence for host-switching, except for bat species sharing day roost sites. These results highlight that strong variation between islands does exist and is associated with the composition of the bat species community on each island. Future studies should investigate whether CoVs detected in these bats have a potential for spillover in other hosts.
View
Bat coronavirus phylogeography in the Western Indian Ocean
Article
Full-text available
  • Apr 2020
Bats provide key ecosystem services such as crop pest regulation, pollination, seed dispersal, and soil fertilization. Bats are also major hosts for biological agents responsible for zoonoses, such as coronaviruses (CoVs). The islands of the Western Indian Ocean are identified as a major biodiversity hotspot, with more than 50 bat species. In this study, we tested 1,013 bats belonging to 36 species from Mozambique, Madagascar, Mauritius, Mayotte, Reunion Island and Seychelles, based on molecular screening and partial sequencing of the RNA-dependent RNA polymerase gene. In total, 88 bats (8.7%) tested positive for coronaviruses, with higher prevalence in Mozambican bats (20.5% ± 4.9%) as compared to those sampled on islands (4.5% ± 1.5%). Phylogenetic analyses revealed a large diversity of α- and β-CoVs and a strong signal of co-evolution between CoVs and their bat host species, with limited evidence for host-switching, except for bat species sharing day roost sites. These results highlight that strong variation between islands does exist and is associated with the composition of the bat species community on each island. Future studies should investigate whether CoVs detected in these bats have a potential for spillover in other hosts.
View
Documented record of Triaenops menamena (family Hipposideridae) in the central highlands of Madagascar
Article
Full-text available
  • Aug 2014
The endemic Malagasy trident bat Triaenops menamena Goodman and Ranivo, 2009, formerly named T. rufus A. Milne-Edwards, 1881 (GOODMAN and RANIVO, 2009), has a broad distribution in the western portion of the island, particularly in areas of sedimentary rock, utilizing caves, rock shelters, and mine shafts for day roosts (GOODMAN, 2011; GOODMAN and RAMASINDRAZANA, 2013). Colony size is known to vary from a few to over 40,000 individuals (CARDIFF, 2006; OLSSON et al., 2006). The elevational range of this species falls from near sea level to about 1000 m (GOODMAN and RAMASINDRAZANA, 2013). However, there are reports of T. menamena from higher elevations, including the Réserve Spéciale d'Ambohitantely in the Central Highlands (RAKOTONDRAMANANA, 2004). While the Ambohitantely record has been cited in the literature on the bats of Madagascar, documentation of this species occurrence at this site is ambiguous and a voucher specimen appears to be lacking. In April 2014, we conducted a biological inventory of the Réserve Spéciale d'Ambohitantely, including documentation of bat species occurring in the Grotte des Chauves-souris (18°10'52.1 " S, 47°17'21.0 " E, 1500 m). This cave is located within the largest remaining forest block (about 1000 ha) in the protected area and in relatively intact montane forest. On 7 April 2014, a single Triaenops menamena was found roosting in the cave (Figure 1) with a group of Miniopterus sp. (Several haplotypes of a small Miniopterus occur in this cave and unnamed species might be present [CHRISTIDIS et al., 2014].) The captured T. menamena was a female that showed no sign of recent reproductive activity. It had a forearm length of 52 mm, falling within the typical range of females of this species given by GOODMAN (2011): 46-53 mm. The animal was collected as a voucher specimen (Field Museum of Natural History [FMNH] SMG-18575). During the same visit to the cave as when the voucher specimen was collected, a second individual of T. menamena was observed roosting with another group of Miniopterus sp. The following day, the cave was revisited and at least one individual of T. menamena was observed amongst a group of Miniopterus sp. We have no evidence that T. menamena breeds at the Grotte des Chauves-souris or anywhere in the immediate vicinity in the Central Highlands. Genetic studies conducted on T. menamena based on about 750 bp of mitochondrial cytochrome b indicate little phylogeographic structure across its broad range on Madagascar (RUSSELL et al. 2007). This species demonstrates largely panmictic genetic structure. This pattern is presumably associated with considerable dispersal and, hence, mixing of genetic pools. Triaenops menamena has been found at a few sites at the fringe of lowland eastern Madagascar, with less than 10 individuals roosting near Tolagnaro (extreme southeast) with a large colony of Rousettus madagascariensis G. Grandidier, 1929 (JENKINS et al., 2007) and in the Parc National de Marojejy (northern central area) (PONT and ARMSTRONG, 1990). Both of these sites are within relatively short distances to dry forest areas where breeding populations of T. menamena are known or suspected to occur. Whether records of this species from Ambohitantely and the lowland eastern sites represent seasonal vagrants, some form of more regular dispersal, or local breeding populations can only be determined by further fieldwork.
View
View
View
The Geology of Madagascar
Chapter
  • Jan 1972
The geological exploration of Madagascar began about a century ago. The beginning was slow, due to the small number of researchers and the modesty of their resources; but research bodies were gradually created with growing facilities. Our present knowledge represents the achievement of numerous geologists, whose work now runs into hundreds of publications, not to mention the impressive archives of the Government services and of state-controlled and private agencies. The task is thus a weighty one, and I am well aware of its difficulties and of the impossibility of presenting anything other than a brief summary of the geology of Madagascar in 1967. I would therefore ask the reader to excuse the inevitably selective and simplified treatment. My hope is to give a general picture of the formation of Madagascar and its problems.
View
View
View
View
View
View
View