Integrative description of two new species of Malagasy chirping giant pill-millipedes, genus Sphaeromimus (Diplopoda: Sphaerotheriida: Arthrosphaeridae)

Leif Moritz, Thomas Wesener

Abstract


The species-rich giant pill-millipedes (Sphaerotheriida) often represent a microendemic component of Madagascar’s mega-invertebrate fauna. Of the chirping genus Sphaeromimus de Saussure & Zehntner, 1902, ten species have been described. Here, we describe two new species of Sphaeromimus integratively, combining light microscopy, scanning electron microscopy, DNA barcoding and micro-CT technology for the first time in a taxonomic description of a giant pill-millipede. S. kalambatritra sp. nov. and S. midongy sp. nov. are the first giant pill-millipedes collected and described from the mountainous rainforests of Kalambatritra and Midongy. Both species show island gigantism compared to their congeners. Our analysis of the mitochondrial COI gene shows that the two species are related to one another with a moderate genetic distance (9.4%), while they are more closely related to an undetermined specimen from the forest of Vevembe (6.3% and 8.4%). They stand in a basal position with S. ivohibe Wesener, 2014 and S. musicus (de Saussure & Zehntner, 1897). The four aforementioned species share a high number of stridulation ribs on the male harp. Our micro-CT analysis provides a look into the head of S. kalambatritra sp. nov. and shows that non-destructive CT methods are a useful tool for studying the inner morphology of giant pill-millipedes.

Keywords


biodiversity; COI; island gigantism; Kalambatritra; Midongy

Full Text:

PDF PDF/A


DOI: https://doi.org/10.5852/ejt.2017.381

References


Akkari N., Enghoff H. & Metscher B.D. 2015. A new dimension in documenting new species: high-detail imaging for myriapod taxonomy and first 3D cybertype of a new millipede species (Diplopoda, Julida, Julidae). PloS One 10 (8): e0135243. https://doi.org/10.1371/journal.pone.0135243

Altschul S.F., Gish W., Miller W., Myers E.W. & Lipman D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology 215 (3): 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

Astrin J.J. & Stüben P.E. 2008. Phylogeny in cryptic weevils: molecules, morphology and new genera of western Palaearctic Cryptorhynchinae (Coleoptera: Curculionidae). Invertebrate Systematics 22 (5): 503–522. https://doi.org/10.1071/IS07057

Blanke A. & Wesener T. 2014. Revival of forgotten characters and modern imaging techniques help to produce a robust phylogeny of the Diplopoda (Arthropoda, Myriapoda). Arthropod Structure & Development 43: 63–75. https://doi.org/10.1016/j.asd.2013.10.003

Bora P., Randriambahiniarime M.O., Rabemananjara F.C.E., Ramilijaona O.R., Glaw F. & Vences M. 2007. A rapid assessment survey of the herpetofauna at Befotaka-Midongy National Park, south-eastern Madagascar. Zoosystematics and Evolution 83 (2): 170–178. https://doi.org/10.1002/mmnz.200700007

Cárcamo H.A., Abe T.A., Prescott C.E., Holl F.B. & Chanway C.P. 2000. Influence of millipedes on litter decomposition, N mineralization, and microbial communities in a coastal forest in British Columbia, Canada. Canadian Journal of Forest Research 30 (5): 817–826. https://doi.org/10.1139/x00-014

Dewar R.E. & Wright H.T. 1993. The culture history of Madagascar. Journal of World Prehistory 7 (4): 417–466. https://doi.org/10.1007/BF00997802

Enghoff H. 2003. Diplopoda, millipedes. In: Goodman S.M. & Benstead J.P. (eds) Natural History of Madagascar: 617–627. University of Chicago Press, Chicago.

Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 (4): 783–791. https://doi.org/10.2307/2408678

Ganzhorn J.U., Lowry P.P., Schatz G.E. & Sommer S. 2001. The biodiversity of Madagascar: one of the world’s hottest hotspots on its way out. Oryx 35 (4): 346–348. https://doi.org/10.1046/j.1365-3008.2001.00201.x

Glaw F. & Verdes M. 2003. Introduction to amphibians. In: Goodman S.M. & Benstead J.P. (eds) Natural History of Madagascar: 883–898. University of Chicago Press, Chicago.

Golovatch S.I., Wesener T., Mauriès J.P. & Semenyuk I.I. 2012. On the identities of Cryxus Leach, 1814 and Zephronia Gray, 1832, the oldest generic names in the millipede order Sphaerotheriida (Diplopoda). Arthropoda Selecta 21 (4): 273–294.

Goodman S.M., Ganzhorn J.U. & Rakotondravony D. 2003. Introduction to mammals. In: Goodman S.M. & Benstead J.P. (eds) Natural History of Madagascar: 1159–1186. University of Chicago Press, Chicago.

Green G.M. & Sussman R.W. 1990. Deforestation history of the eastern rain forests of Madagascar from satellite images. Science 248 (4952): 212–215. https://doi.org/10.1126/science.248.4952.212

Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Sympsoium 41: 95–98.

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 (4): 325–333.

https://doi.org/10.1017/S0376892907004262

Hebert P.D. & Gregory T.R. 2005. The promise of DNA barcoding for taxonomy. Systematic Biology 54 (5): 852–859. https://doi.org/10.1080/10635150500354886

Hebert P.D., Cywinska A. & Ball S.L. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B: Biological Sciences 270 (1512): 313–321. https://doi.org/10.1098/rspb.2002.2218

Hijmans R.J., Guarino L., Cruz M. & Rojas E. 2001. Computer tools for spatial analysis of plant genetic resources data: 1. DIVA-GIS. Plant Genetic Resources Newsletter 127: 15–19.

Horning N.R. 2012. Debunking three myths about Madagascar’s deforestation. Madagascar Conservation and Development 7 (3): 116–119. https://doi.org/10.4314/mcd.v7i3.3

Irwin M.T., Samonds K.E. & Raharison J.L. 2001. A biological inventory of the lemur community of Réserve Spéciale de Kalambatritra, South-Central Madagascar. Lemur News 6: 24–28.

Jeekel C.A.W. 1999. A new pill-millipede from Madagascar, with a catalogue of the species hitherto described from the island (Diplopoda, Sphaerotheriida). Myriapod Memoranda 1: 5–20

Klopfstein S., Kropf C. & Quicke D.L.J. 2010. An evaluation of phylogenetic informativeness profiles and the molecular phylogeny of Diplazontinae (Hymenoptera, Ichneumonidae). Systematic Biology 59 (2): 226–241. https://doi.org/10.1093/sysbio/syp105

Limaye A. 2012. Drishti: a volume exploration and presentation tool. SPIE Proceedings Developments in X-Ray Tomography 8 85060X. https://doi.org/10.1117/12.935640

Moat J. & Smith P. 2007. Atlas of the Vegetation of Madagascar. Royal Botanic Gardens, Kew, Richmond, Surrey.

Myers N., Mittermeier R.A., Mittermeier C.G., da Fonseca A.B. & Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 491 (333): 853–858. https://doi.org/10.1038/35002501

Oatley C.W., Nixon W.C. & Pease R.F.W. 1966. Scanning electron microscopy. Advances in Electronics and Electron Physics 21: 181–247. https://doi.org/10.1016/S0065-2539(08)61010-0

Padial J.M., Miralles A., De La Riva I. & Vences M. 2010. The integrative future of taxonomy. Frontiers in Zoology 7 (1): 1–14. https://doi.org/10.1186/1742-9994-7-16

Raxworthy C.J. 2003. Introduction to reptiles. In: Goodman S.M. & Benstead J.P. (eds) Natural History of Madagascar: 934–949. University of Chicago Press, Chicago.

Ritman E.L. 2004. Micro-computed tomography – current status and developments. Annual Review of Biomedical Engineering 6: 185–208. https://doi.org/10.1146/annurev.bioeng.6.040803.140130

Sanger F., Nicklen S. & Coulson A.R. 1977. DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences 74 (12): 5463–5467. https://doi.org/10.1073/pnas.74.12.5463

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J., White D.J., Hartenstein V., Eliceiri K., Tomancak P. & Cardona A. 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9 (7): 676–682. https://doi.org/10.1038/nmeth.2019

Shear W.A. & Edgecombe G.D. 2010. The geological record and phylogeny of the Myriapoda. Arthropod Structure & Development 39: 174–190. https://doi.org/10.1016/j.asd.2009.11.002

Shelley R.M. & Golavatch S.I. 2011. Atlas of myriapod biogeography. I. Indigenous ordinal and supra-ordinal distributions in the Diplopoda: Perspectives on taxon origins and ages, and a hypothesis on the origin and early evolution of the class. Insecta Mundi 158: 1–134.

Silvestri F. 1903. Classis Diplopoda. Vol. 1, Anatome. Pars 1a, Segmenta, Tegumentum, Musculi. Della Torre, Portici, Italy.

Tamura K. & Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

Tamura K., Stecher G., Peterson D., Filipski A. & Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.

https://doi.org/10.1093/molbev/mst197

Tavaré S. 1986. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures on Mathematics in the Life Sciences 17: 57–86.

Townsend J.P. & Leuenberger C. 2011. Taxon sampling and the optimal rates of evolution for phylogenetic inference. Systematic Biology 60 (3): 358–365. https://doi.org/10.1093/sysbio/syq097

Verhoeff K. 1932. Diplopoda. In: Verhoeff K. (ed.) Bronns Klassen und Ordnungen des Tierreichs, Bd. 5/II. Akademische Verlagsgesellschaft, Leipzig.

Waeber P.O., Wilmé L., Mercier J.R., Camara C. & Lowry II P.P. 2016. How effective have thirty years of internationally driven conservation and development efforts been in Madagascar? PloS One 11 (8): e0161115. https://doi.org/10.1371/journal.pone.0161115

Wells N.A. 2003. Some hypotheses on the Mesozoic and Cenozoic paleoenvironmental history of Madagascar. In: Goodman S.M. & Benstead J.P. (eds) Natural History of Madagascar: 16–34. University of Chicago Press, Chicago.

Wesener T. 2009. Unexplored richness: discovery of 31 new species of giant pill-millipedes endemic to Madagascar, with a special emphasis on microendemism (Diplopoda, Sphaerotheriida). Zootaxa 2097: 1–131.

Wesener T. 2014a. Redescription of Polyzonium malagassum, a new synonym of Rhinotus purpureus (Pocock, 1894), with notes about the occurrence of the order Polyzoniida on Madagascar (Diplopoda). Zootaxa 3790 (4): 587–594. https://doi.org/10.11646/zootaxa.3790.4.7

Wesener T. 2014b. First records of the order Siphonophorida from Madagascar and Mauritius (Diplopoda). Revue Suisse de Zoologie 121 (3): 415–423. Available from https://biodiversitylibrary.org/page/52965457 [accessed 14 Nov. 2017].

Wesener T. 2014c. A new phylogenetic analysis of the Sphaerotheriida (Diplopoda) with a revision of the Australian giant pill-millipedes. Invertebrate Systematics 28 (2): 196–213. https://doi.org/10.1071/IS13048

Wesener T. 2015. No millipede endemics north of the Alps? DNA-barcoding reveals Glomeris malmivaga Verhoeff, 1912 as a synonym of G. ornata Koch, 1847 (Diplopoda, Glomerida, Glome-ridae). Zootaxa 3999 (4): 571–580. https://doi.org/10.11646/zootaxa.3999.4.7

Wesener T. 2016. The giant pill-millipedes, order Sphaerotheriida – An annotated species catalogue with morphological atlas and list of apomorphies (Arthropoda: Diplopoda). Bonn Zoological Bulletin Supplementum 63: 1–104.

Wesener T. & Sierwald P. 2005. The giant pill-millipedes of Madagascar - Revision of the genus Sphaeromimus. Proceedings of the California Academy of Science 56: 557–599.

Wesener T. & VandenSpiegel D. 2009. A first phylogenetic analysis of giant pill-millipedes (Diplopoda: Sphaerotheriida), a new model Gondwanan taxon, with special emphasis on island gigantism. Cladistics 25: 545–573. https://doi.org/10.1111/j.1096-0031.2009.00267.x

Wesener T. & Wägele J.W. 2008. The giant pill-millipedes of Madagascar: revision of the genus Zoosphaerium (Myriapoda, Diplopoda, Sphaerotheriida). Zoosystema 30 (1): 5–82.

Wesener T., Enghoff H. & Sierwald P. 2009a. Review of the Spirobolida on Madagascar, with descriptions of twelve new genera, including three genera of ‘fire millipedes’ (Diplopoda). Zookeys 19: 1–128. https://doi.org/10.3897/zookeys.19.221

Wesener T., Enghoff H., Hoffmann R.L., Wägele J.W. & Sierwald P. 2009b. Revision of the endemic giant fire millipedes of Madagascar, genus Aphistogoniulus (Diplopoda: Spirobolida: Pachybolidae). International Journal of Myriapodology 2 (1): 15–52. https://doi.org/10.1163/187525409X462403

Wesener T., Raupach M.J. & Sierwald P. 2010. The origins of the giant pill-millipedes from Madagascar (Diplopoda: Sphaerotheriida: Arthrosphaeridae). Molecular Phylogenetics and Evolution 57 (3): 1184–1193. https://doi.org/10.1016/j.ympev.2010.08.023

Wesener T., Köhler J., Fuchs S. & VandenSpiegel D. 2011. How to uncoil your partner—“mating songs” in giant pill-millipedes (Diplopoda: Sphaerotheriida). Naturwissenschaften 98 (11): 967–975. https://doi.org/10.1007/s00114-011-0850-8

Wesener T., Minh-Tu Le D. & Loria S.F. 2014. Integrative revision of the giant pill-millipede genus Sphaeromimus, with the description of seven new species (Diplopoda, Sphaerotheriida, Arthro-sphaeridae). ZooKeys 414: 67–104. https://doi.org/10.3897/zookeys.414.7730

Wongthamwanich N., Panha S., Sierwald P., Wesener T. & Thirakhupt K. 2012. A new species of the giant pill-millipede genus Sphaerobelum Verhoeff, 1924 from northern Thailand, with an extensive description and molecular characters (Diplopoda: Sphaerotheriida: Zephroniidae). Zootaxa 3220: 29–43.

Yushkevich P.A., Piven J., Hazlett H.C., Smith R.G., Ho S., James C., Gee J.C. & Gerig G. 2006. User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. Neuroimage 31 (3): 1116–1128. https://doi.org/10.1016/j.neuroimage.2006.01.015


Refbacks

  • There are currently no refbacks.


License URL: https://creativecommons.org/licenses/by/3.0/