Taxonomic anarchy or an inconvenient truth for conservation? Accelerated species discovery reveals evolutionary patterns and heightened extinction threat in Afro-Malagasy small mammals

References

ACR. 2017. African Chiroptera Report 2017. AfricanBats NPC, Pretoria.Search in Google Scholar

Artyushin, I.V., A.A. Bannikova, V.S. Lebedev and S.V. Kruskop. 2009. Mitochondrial DNA relationships among North Palaearctic Eptesicus (Vespertilionidae, Chiroptera) and past hybridization between Common Serotine and Northern Bat. Zootaxa 2262: 40–52.10.11646/zootaxa.2262.1.2Search in Google Scholar

Baxter, R., P. Taylor and M.F. Child. 2017. Otomys auratus. The IUCN Red List of Threatened Species 2017: e.T110662638A110662647. http://dx.doi.org/10.2305/IUCN.UK.2017-2.RLTS.T110662638 A110662647.en. Downloaded on 15 October 2017.Search in Google Scholar

Bohmann, L. 1952. Die afrikanische Nagergattung Otomys F. Cuvier. Z. Säugetierk. 18: 1–80.Search in Google Scholar

Bryja, J., V. Mazoch, H. Patzenhauerová, C. Mateke, J. Zima Jr., J. Šklíba and R. Šumbera. 2012. Revised occurrence of rodents from the tribe Praomyini (Muridae) in Zambia based on mitochondrial DNA analyses: implications for biogeography and conservation. Folia Zool. 61: 268–283.10.25225/fozo.v61.i3.a11.2012Search in Google Scholar

Burgin, C.J., J.P. Colella, P.L. Kahn and N.S. Upham. 2018. How many species of mammals are there? J. Mammal. 99: 1–14.10.1093/jmammal/gyx147Search in Google Scholar

Carleton, M.D. and E.S. Byrne. 2006. The status Otomys orestes dollmani Heller, 1912 (Muridae: Otomyinae), a rodent described from the Mathews Range, central Kenya. Proc. Biol. Soc. Wash. 119: 477–515.10.2988/0006-324X(2006)119[477:TSOOOD]2.0.CO;2Search in Google Scholar

Carleton, M.D. and S.M. Goodman. 2007. A new species of the Eliurus majori complex (Rodentia: Muroidea: Nesomyidae) from south-central Madagascar, with remarks on emergent species groupings in the genus Eliurus. Am. Mus. Novit. 3547: 1–21.10.1206/0003-0082(2007)3547[1:ANSOTE]2.0.CO;2Search in Google Scholar

Carleton, M.D. and W.T. Stanley. 2005. Review of the Hylomyscus denniae complex (Rodentia: Muridae) in Tanzania, with a description of a new species. Proc. Natl. Acad. Sci. USA 118: 619–646.10.2988/0006-324X(2005)118[619:ROTHDC]2.0.CO;2Search in Google Scholar

Carleton, M.D., R.A. Banasiak and W.T. Stanley. 2015. A new species of the rodent genus Hylomyscus from Angola, with a distributional summary of the H. anselli species group (Muridae: Murinae: Praomyini). Zootaxa 4040: 101–128.10.11646/zootaxa.4040.2.1Search in Google Scholar

Ceríaco, L.M P., E.E. Gutiérrez and A. Dubois. 2017. Photography-based taxonomy is inadequate, unnecessary, and potentially harmful for biological sciences. Zootaxa 4196: 435–445.10.11646/zootaxa.4196.3.9Search in Google Scholar

Child, M.F., D. Raimondo, E. Do Linh San, L. Roxburgh and H. Davies-Mostert. 2016. The Red List of mammals of South Africa, Swaziland and Lesotho. South African National Biodiversity Institute and Endangered Wildlife Trust, South Africa.Search in Google Scholar

Christidis, L., S.M. Goodman, K. Naughton and B. Appleton. 2014. Insights into the evolution of a cryptic radiation of bats: dispersal and ecological radiation of Malagasy Miniopterus (Chiroptera: Miniopteridae). PLoS One 9: e92440.10.1371/journal.pone.0092440Search in Google Scholar PubMed

Cohen, L., P. Taylor, D. Jacobs, T. Kearney, K. MacEwan, A. Monadjem, L.R. Richards, C. Schoeman and T. Sethusa. 2017. Rhinolophus cohenae. The IUCN Red List of Threatened Species 2017: e.T64587154A64587542. http://dx.doi.org/10.2305/IUCN.UK.2017-2.RLTS.T64587154A64587542.en. Downloaded on 15 October 2017.10.2305/IUCN.UK.2017-2.RLTS.T64587154A64587542.enSearch in Google Scholar

Cotterill, F.P.D. 2002. The future of Natural Science Collections into the 21st Century. Conferencia de Clausura. In: Actas del I Simposio sobre el Patrimonio Natural en las Colecciones Públicas en España (Vitoria, 25–27 Septiembre 2001). Departamento de Cultura, Diputación Foral de Alava. Vitoria. pp. 237–282. ISBN: 84-7821-497-6.Search in Google Scholar

Cotterill. F.P.D. 2003. Species concepts and the real diversity of antelopes. In: (A. Plowman, ed.) Ecology and Conservation of Mini-antelope: Proceedings of an International Symposium on Duiker and Dwarf Antelope in Africa. Filander Verlag, Fürth. pp. 59–118.Search in Google Scholar

Cotterill, F.P.D. 2016. The tentelic thesis, interdisciplinarity, and earth system science: how natural history collections underpin geobiology. Arch. Zool. Mus. Lomonosov Mos. Stat. Univ. 54: 598–635.Search in Google Scholar

Cotterill, F.P., P.J. Taylor, S. Gippoliti, J.M. Bishop and C.P. Groves. 2014. Why one century of phenetics is enough: response to “Are there really twice as many bovid species as we thought?” Syst. Biol. 63: 819–832.10.1093/sysbio/syu003Search in Google Scholar PubMed

Cotterill, F.P. D., C.P. Groves and P.J. Taylor. 2017. Taxonomy: refine rather than stabilize. Nature 547: 162.10.1038/547162dSearch in Google Scholar PubMed

Demos, T.C., B. Agwanda and M.J. Hickerson. 2014. Integrative taxonomy within the Hylomyscus denniae complex (Rodentia: Muridae) and a new species from Kenya. J. Mammal. 95: E1–E15.10.1644/13-MAMM-A-268Search in Google Scholar

Denys, C., A.D. Missoup, V. Nicolas, O. Fülling, A. Delapré, C.F. Bilong Bilong, P.J. Taylor and R. Hutterer. 2014. African highlands as mammal diversity hotspots: new records of Lamottemys okuensis Petter, 1986 (Rodentia: Muridae) and other endemic rodents from Mt Oku, Cameroon. Zoosystema 36: 647–690.10.5252/z2014n3a6Search in Google Scholar

Engelbrecht, A., P.J. Taylor, S.R. Daniels and R.V. Rambau. 2011. Cryptic speciation in the southern African vlei rat, Otomys irroratus complex: evidence derived from mitochondrial cyt b and niche modeling. Biol. J. Linn. Soc. 104: 192–206.10.1111/j.1095-8312.2011.01696.xSearch in Google Scholar

Fenton, M.B. and N.B. Simmons. 2015. Bats, a world of science and mystery. The University of Chicago Press, Chicago.10.7208/chicago/9780226065267.001.0001Search in Google Scholar

Friedman, Y. and B. Daly. 2004. Red Data Book of the mammals of South Africa: a conservation assessment. Conservation Specialist Group (SSC/IUCN), Endangered Wildlife Trust, Johannesburg.Search in Google Scholar

Frost, D.R. and A.G. Kluge. 1994. A consideration of epistemology in systematic biology, with special reference to species. Cladistics 10: 259–294.10.1111/j.1096-0031.1994.tb00178.xSearch in Google Scholar

Garnett, S.T. and L. Christidis. 2017. Taxonomy anarchy hampers conservation. Nature 546: 25–27.10.1038/546025aSearch in Google Scholar PubMed

Ghiselin, M.T. 1974. A radical solution to the species problem. Syst. Zool. 23: 536–544.10.2307/2412471Search in Google Scholar

Ghiselin, M.T. 2002. Species concepts: the basis for controversy and reconciliation. Fish Fish. 3: 151–160.10.1046/j.1467-2979.2002.00084.xSearch in Google Scholar

Gippoliti, S. and C.P. Groves. 2012. “Taxonomic inflation” in the historical context of mammalogy and conservation. Hystrix, It. J. Mamm. 23: 6–9.Search in Google Scholar

Gippoliti, S., F.P.D. Cotterill, D. Zinner and C.P. Groves. 2018. Impacts of taxonomic inertia for the conservation of African ungulate diversity: an overview. Biol. Rev. 93: 115–130.10.1111/brv.12335Search in Google Scholar PubMed

Goodman, S. and A. Monadjem. 2017. Family Nesomyidae (pouched rats, climbing mice and fat mice). In: (D.E. Wilson, T.E. Lacher, Jr and R.A. Mittermeier, eds.) Handbook of the mammals of the world. Vol. 7. Rodents II. Lynx Edicions, Barcelona. pp. 156–203.Search in Google Scholar

Goodman, S.M., K.E. Ryan, C.P. Maminirina, J. Fahr, L. Christidis and B. Appleton. 2007. The specific status of populations on Madagascar referred to Miniopterus fraterculus (Chiroptera: Vespertilionidae), with description of a new species. J. Mammal. 88: 1216–1229.10.1644/06-MAMM-A-285R1.1Search in Google Scholar

Goodman, S.M., H.M. Bradman, C.P. Maminirina, K.E. Ryan, L. Christidis and B. Appleton. 2008. A new species of Miniopterus (Chiroptera: Miniopteridae) from lowland southeastern Madagascar. Mamm. Biol. 73: 199–213.10.1016/j.mambio.2007.12.003Search in Google Scholar

Goodman, S.M., C.P. Maminirina, N. Weyeneth, H.M. Bradman, L. Christidis, M. Ruedi and B. Appleton. 2009a. The use of molecular and morphological characters to resolve the taxonomic identity of cryptic species: the case of Miniopterus manavi (Chiroptera, Miniopteridae). Zool. Scr. 38: 339–363.10.1111/j.1463-6409.2008.00377.xSearch in Google Scholar

Goodman, S.M., C.P. Maminirina, H.M. Bradman, L. Christidis and B. Appleton. 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. Am. Mus. Novit. 3669: 1–33.10.1206/652.1Search in Google Scholar

Goodman, S.M., M. Raheriarisena and S.A. Jansa. 2009c. A new species of Eliurus Milne Edwards, 1885 (Rodentia: Nesomyinae) from the Réserve Spéciale d’Ankarana, northern Madagascar. Bonn. Zool. Beitr. 56: 133–149.Search in Google Scholar

Goodman, S.M., C.P. Maminirina, H.M. Bradman, L. Christidis and B. Appleton. 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. J. Zoolog. Syst. Evol. Res. 48: 75–86.10.1111/j.1439-0469.2009.00524.xSearch in Google Scholar

Goodman, S.M., B. Ramasindrazana, C.P. Maminirina, M.C. Schoeman and B. Appleton. 2011. Morphological, bioacoustical, and genetic variation in Miniopterus bats from eastern Madagascar, with the description of a new species. Zootaxa 2880: 1–19.10.11646/zootaxa.2880.1.1Search in Google Scholar

Goodman, S.M., B. Ramasindrazana, K.M. Naughton and B. Appleton. 2015. Description of a new species of the Miniopterus aelleni group (Chiroptera: Miniopteridae) from upland areas of central and northern Madagascar. Zootaxa 3936: 538–558.10.11646/zootaxa.3936.4.4Search in Google Scholar PubMed

Groves, C. and P. Grubb. 2011. Ungulate taxonomy. The Johns Hopkins University Press, Baltimore, MD.10.56021/9781421400938Search in Google Scholar

Groves, C.P., F.P.D. Cotterill, S. Gippoliti, J. Robovský, C. Roos, P. Taylor and D. Zinner. 2017. Species definitions and conservation: a review and case studies from African mammals. Conserv. Genet. 18: 1247–1256.10.1007/s10592-017-0976-0Search in Google Scholar

Happold, D.C.D. (ed.). 2013. Mammals of Africa. Volume III: Rodents, hares and rabbits. Bloomsbury Publishing, London.Search in Google Scholar

Happold, M. and D.C.D. Happold (eds.). 2013. Mammals of Africa. Volume IV: Hedgehogs, shrews and bats. Bloomsbury Publishing, London.Search in Google Scholar

Hausdorf, B. 2011. Progress toward a general species concept. Evolution 65: 923–931.10.1111/j.1558-5646.2011.01231.xSearch in Google Scholar PubMed

Heller, R., P. Frandsen, E.D. Lorenzen and H.R. Siegismund. 2013. Are there really twice as many bovid species as we thought? Syst. Biol. 62: 490–493.10.1093/sysbio/syt004Search in Google Scholar PubMed

Heller, R., P. Frandsen, E.D. Lorenzen and H.R. Siegismund. 2014. Is diagnosability an indicator of speciation? Response to “Why one century of phenetics is enough”. Syst. Biol. 63: 833–837.10.1093/sysbio/syu034Search in Google Scholar PubMed

Hennig, W. 1966. Phylogenetic systematics. Translated by D. D. David and R. Zangerl. University of Illinois Press, Urbana.Search in Google Scholar

Hoffmann, M.P., P. Grubb, C.P. Groves, R. Hutterer, R.E. van der Straeten, N. Simmons and W. Bergmans. 2009. A synthesis of African and western Indian Ocean Island mammal taxa (Class: Mammalia) described between 1988 and 2008: an update to Allen (1939) and Ansell (1989). Zootaxa 2205: 1–36.10.11646/zootaxa.2205.1.1Search in Google Scholar

Honacki, J.H., K.E. Kinman and J.W. Koeppl. 1982. Mammal Species of the World: a taxonomic and geographic reference. Allen Press, Lawrence, Kansas.Search in Google Scholar

Isaac, N.J., J. Mallet and G.M. Mace. 2004. Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol. Evol. 19: 464–469.10.1016/j.tree.2004.06.004Search in Google Scholar PubMed

IUCN/SSC Antelope Specialist Group 2017. Taxonomy Policy. Version 2.0. IUCN/SSC Antelope Specialist Group.Search in Google Scholar

Khan, F.A.A., C.D. Phillips and R.J. Baker. 2014. Timeframes of speciation, reticulation, and hybridization in the bulldog bat explained through phylogenetic analyses of all genetic transmission elements. Syst. Biol. 63: 96–110.10.1093/sysbio/syt062Search in Google Scholar PubMed

Kitchener, A.C., C. Eizirik, E. Breitenmoser-Wursten, A. Gentry, L. Werdelin, A. Wilting, N. Yamaguchi, A.V. Abramov, P. Christiansen, C. Driscoll, J.W. Duckworth, W. Johnson, S.-J. Luo, E. Meijaard, P. O’Donoghue, J. Sanderson, K. Seymour, M. Bruford, C. Groves M. Hoffmann, K. Nowell. Z. Timmons and S. Tobe. 2017. A revised taxonomy of the Felidae. The final report of the Cat Classification Task Force of the IUCN/SSC Cat Specialist Group. Cat News Special Issue 11, pp. 80.Search in Google Scholar

Lavrenchenko, L.A., E. Verheyen, S.G. Potapov, V.S. Lebedev, N.S. Bulatova, V.M. Aniskin, W.N. Verheyen and A.P. Ryskov. 2004. Divergent and reticulate processes in evolution of Ethiopian Lophuromys flavopunctatus species complex: evidence from mitochondrial and nuclear DNA differentiation patterns. Biol. J. Linn. Soc. 83: 301–316.10.1111/j.1095-8312.2004.00390.xSearch in Google Scholar

Lavrenchenko, L.A., W.N. Verheyen, E. Verheyen, J. Hulselmans and H. Leirs. 2007. Morphometric and genetic study of Ethiopian Lophuromys flavopunctatus Thomas, 1888 species complex with description of three new 70-chromosomal species (Muridae, Rodentia). Bull. Inst. R. Sci. N B-S 77: 77–117.Search in Google Scholar

Mayden, R.L. 1997. Chap. 19. A hierarchy of species concepts: the denouement in the saga of the species problem. In (M.F. Oaridge, H.A. Dawah and M.R. Wilson, eds.) Species: the units of biodiversity. Chapman & Hall, London, New York. pp. 381–424.Search in Google Scholar

Mayden, R.J. 1999. Consilience and a hierarchy of species concepts: advances towards closure on the species puzzle. J. Nematol. 31: 95–116.Search in Google Scholar

Monadjem, A., P.J. Taylor, F.P.D. Cotterill and M.C. Schoeman. 2010. Bats of southern and south-central Africa: a biogeographic and taxonomic synthesis. Wits University Press, Johannesburg.Search in Google Scholar

Monadjem, A., S.M. Goodman, W.T. Stanley and B. Appleton. 2013. A cryptic new species of Miniopterus from south-eastern Africa based on molecular and morphological characters. Zootaxa 3746: 123–142.10.11646/zootaxa.3746.1.5Search in Google Scholar PubMed

Monadjem, A., P.J. Taylor, C. Denys and F.P.D. Cotterill. 2015. Rodents of Sub-Saharan Africa: a biogeographic and taxonomic synthesis. De Gruyter, Berlin.10.1515/9783110301915Search in Google Scholar

Monadjem, A., L. Richards and C. Denys. 2016. An African bat hotspot: the importance of Mount Nimba for bat diversity. Acta Chiropterol. 18: 359–375.10.3161/15081109ACC2016.18.2.005Search in Google Scholar

Nesi, N., E. Nakoune, C. Cruaud and A. Hassanin. 2011. DNA barcoding of African fruit bats (Mammalia, Pteropodidae). The mitochondrial genome does not provide a reliable discrimination between Epomophorus gambianus and Micropteropus pusillus. C.R. Biol. 334: 544–554.10.1016/j.crvi.2011.05.003Search in Google Scholar PubMed

Puechmaille, S.J., B. Allegrini, P. Benda, K. Gürün, J. Šrámek, C. Ibañez, J. Juste and R. Bilgin. 2014. A new species of the Miniopterus schreibersii species complex (Chiroptera: Miniopteridae) from the Maghreb Region, North Africa. Zootaxa 3794: 108–124.10.11646/zootaxa.3794.1.4Search in Google Scholar PubMed

Raposo, M.A., R. Stopiglia, G.R.R. Brito, F.A. Bockmann, G.M. Kirwan, J. Gayon and A. Dubois. 2017. What really hampers taxonomy and conservation? A riposte to Garnett and Christidis (2017). Zootaxa 4317: 179–184.10.11646/zootaxa.4317.1.10Search in Google Scholar

Schoeman, M.C., F.P.D. Cotterill, P.J. Taylor and A. Monadjem. 2013. Using potential distributions to explore environmental correlates of bat species richness in southern Africa: effects of model selection and taxonomy. Curr. Zool. 59: 279–293.10.1093/czoolo/59.3.279Search in Google Scholar

Simpson, G.G. 1940. Types in modern taxonomy. Am. J. Sci. 238: 413–431.10.2475/ajs.238.6.413Search in Google Scholar

Taylor, P. 2017. Rhinolophus smithersi. The IUCN Red List of Threatened Species 2017: e.T64588371A64589277. http://dx.doi.org/10.2305/IUCN.UK.2017-2.RLTS.T64588371A64589277.en. Downloaded on 15 October 2017.10.2305/IUCN.UK.2017-2.RLTS.T64588371A64589277.enSearch in Google Scholar

Taylor, P.J., S. Maree, J. Sandwyk, R. Baxter and R.V. Rambau. 2009. When is a species not a species? Uncoupled phenotypic, karyotypic and genotypic divergence in two species of South African laminate-toothed rats (Murinae: Otomyini). J. Zool. (Lond.) 277: 317–332.10.1111/j.1469-7998.2008.00542.xSearch in Google Scholar

Taylor, P.J., L.A. Lavrenchenko, M.D. Carleton, E. Verheyen, N. Bennett, C. Oosthuisen and S. Maree. 2011. Specific limits and emerging diversity patterns in east African populations of laminate-toothed rats, genus Otomys (Muridae: Murinae: Otomyini): Revision of the Otomys typus complex. Zootaxa 3024: 1–66.10.11646/zootaxa.3024.1.1Search in Google Scholar

Taylor, P.J., S. Stoffberg, A. Monadjem, M.C. Schoeman, J. Bayliss and F.P.D. Cotterill. 2012. Four new bat species (Rhinolophus hildebrandtii complex) reflect Plio-Pleistocene divergence of dwarfs and giants across an Afromontane Archipelago. PLoS One 7: e41744.10.1371/journal.pone.0041744Search in Google Scholar PubMed PubMed Central

Taylor, P.J., T.C. Kearney, J.C. Kerbis Peterhans, R.M. Baxter and S. Willows-Munro. 2013. Cryptic diversity in forest shrews of the genus Myosorex from southern Africa, with the description of a new species and comments on M. tenuis. Zool. J. Linn. Soc. 169: 881–902.10.1111/zoj.12083Search in Google Scholar

Taylor, P.J., S. Maree, F.P.D. Cotterill, A.D.V. Missoup, V. Nicolas and C. Denys. 2014. Molecular and morphological evidence for a Pleistocene radiation of laminate-toothed rats (Otomys: Rodentia) across a volcanic archipelago in equatorial Africa. Biol. J. Linnean Soc. 113: 320–344.10.1111/bij.12317Search in Google Scholar

Taylor, P.J., A. Munyai, I. Gaigher and R. Baxter. 2015. Afromontane small mammals do not follow the hump-shaped rule: elevational variation in a tropical biodiversity hotspot (Soutpansberg Mountains, South Africa). J. Trop. Ecol. 31: 37–48.10.1017/S0266467414000613Search in Google Scholar

Taylor, P.J., A. Nengovhela, J. Linden and R.M. Baxter. 2016. Past, present and future distribution of Afromontane rodents (Muridae: Otomys) reflect climate-change predicted biome changes. Mammalia 80: 359–375.10.1515/mammalia-2015-0033Search in Google Scholar

Vallo, P., P. Benda, J. Ĉervený and P. Koubek. 2013. Conflicting mitochondrial and nuclear paraphyly in small-sized West African house bats (Vespertilionidae). Zool. Scripta 42: 1–12.10.1111/j.1463-6409.2012.00563.xSearch in Google Scholar

Verheyen, W.N., J.L.J. Hulselmans, T. Dierckx, L. Mulungu, H. Leirs, M. Corti and E. Verheyen. 2007. The characterization of the Kilimanjaro Lophuromys aquilus TRUE 1892 population and the description of five new Lophuromys species (Rodentia, Muridae). Bull. Inst. R. Sci. N B-S 77: 23–75.Search in Google Scholar

Wiley, E.O. 1978. The evolutionary species concept reconsidered. Syst. Zool. 27: 17–26.10.2307/2412809Search in Google Scholar

Wilson, D.E. and D.M. Reeder (eds.). 1993. Mammal species of the World: a taxonomic and geographic reference. 2nd ed. Smithsonian Institution Press, Washington, DC.Search in Google Scholar

Wilson, D.E. and D.M. Reeder (eds.). 2005. Mammal species of the World: a taxonomic and geographic reference. 3rd ed. The Johns Hopkins University Press, Baltimore.Search in Google Scholar

Wilson, D.E., T.E. Lacher, Jr., and R.A. Mittermeier (eds.). 2016. Handbook of the mammals of the world. Vol. 6. Rodents I. Lynx Edicions, Barcelona.Search in Google Scholar

Wilson, D.E., T.E. Lacher, Jr., and R.A. Mittermeier (eds.). 2017. Handbook of the mammals of the World. Vol. 7. Rodents II. Lynx Edicions, Barcelona.Search in Google Scholar

Zachos, F.E., M. Apollonio, E.V. Bärmann, M. Festa-Bianchet, U. Göhlich, J.C. Habel, E. Haring, L. Kruckenhauser, S. Lovari, A.D. McDevitt, C. Pertoldi, G.E. Rössner, M.R. Sánchez-Villagra, M. Scandura and F. Suchentrunk. 2013. Species inflation and taxonomic artefacts – a critical comment on recent trends in mammalian classification. Mamm. Biol. 78: 1–6.10.1016/j.mambio.2012.07.083Search in Google Scholar