Description of a new haemadipsid species of genus Chtonobdella from Ranomafana National Park using micro-computed tomography

Authors

Keywords:

Leech, new species, Haemadipsidae, sp. nov., Madagascar, cox1 molecular barcoding, Duognathous leeches, iDNA

Abstract

The terrestrial blood feeding leeches of Madagascar represent an understudied group with recent evidence for cryptic diversity. By combining genetic and morphological data including cox1 molecular barcoding and micro-computed tomography (mCT) imaging, we present evidence for the presence of a new species in the genus Chtonobdella Grube, 1866. This description includes, for the first time, mCT rendering of known leech species from Madagascar, which were previously described solely by dissection.

 

Résumé

Les sangsues terrestres hématophages de Madagascar constituent un groupe qui reste encore peu étudié en même temps que des indices récents pointent vers une diversité cryptique. En combinant des données génétiques et morphologiques, incluant le codage moléculaire par le gène cox1 et l’imagerie par micro-tomodensitométrie (µCT), nous apportons des éléments attestant de la présence d’une nouvelle espèce au sein du genre Chtonobdella Grube, 1866. Cette description inclut, pour la première fois, une visualisation µCT d’espèces de sangsues connues de Madagascar, auparavant décrites uniquement par dissection.

Author Biographies

Mai Fahmy, Fordham University, American Museum of Natural History

1. Department of Biological Sciences, Fordham University, 441 East Fordham Road, Bronx, NY 10458, USA

2. American Museum of Natural History, 200 Central Park W, New York, NY 10024, USA

Ny Anjara Fifi Ravelomanantsoa, University of Antananarivo

Ambohitsaina, Antananarivo 101

Aimé Victor Tombotiana, Centre ValBio

BP 33, Ranomafana, Ifanadiana 312

Evon Hekkala, Fordham University, American Museum of Natural History

1. Department of Biological Sciences, Fordham University, 441 East Fordham Road, Bronx, NY 10458, USA

2. American Museum of Natural History, 200 Central Park W, New York, NY 10024, USA

References

Apakupakul, K., Siddall, M. E. and Burreson, E. M. 1999. Higher level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and gene sequences. Molecular Phylogenetics and Evolution 12, 3: 350–359. <https://doi.org/10.1006/mpev.1999.0639>

Blanchard, R. 1917. Monographie des hémadipsines (sangsues terrestres). Bulletin de la Société de Pathologie Exotique 10: 640–675. Available online <https://archive.org/details/BIUSante_bspex1917/page/639/mode/2up>

Borda, E. 2006. A revision of the Malagabdellinae (Arhynchobdellida: Domanibdellidae), with a description of a new species, Malagabdella niarchosorum, from Ranomafana National Park, Madagascar. American Museum Novitates 3531: 1–13. <https://doi.org/10.1206/0003-0082(2006)3531[1:AROTMA]2.0.CO;2>

Borda, E. and Siddall, M. E. 2011. Insights into the evolutionary history of Indo-Pacific bloodfeeding terrestrial leeches (Hirudinida:Arhynchobdellida:Haemadipisdae). Invertebrate Systematics 24, 5: 456–472. <https://doi.org/10.1071/IS10013>

Borda, E., Oceguera-Figueroa, A. and Siddall, M. E. 2008. On the classification, evolution and biogeography of terrestrial haemadipsoid leeches (Hirudinida: Arhynchobdellida: Hirudiniformes). Molecular Phylogenetics and Evolution 46, 1: 142–154. <https://doi.org/10.1016/j.ympev.2007.09.006>

Darriba, D., Taboada, G. L., Doallo, R. and Posada, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772. <https://doi.org/10.1038/nmeth.2109>

Drinkwater, R., Jucker, T., Potter, J. H. T., Swinfield, T., Coomes, D. A., et al. 2021. Leech blood-meal invertebrate-derived DNA reveals differences in Bornean mammal diversity across habitats. Molecular Ecology 30, 3: 3299–3312. <https://doi.org/10.1111/MEC.15724>

Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 5: 1792–1797. <https://doi.org/10.1093/NAR/GKH340>

Fahmy, M., Ravelomanantsoa, N. A. F., Youssef, S., Hekkala, E. and Siddall, M. 2019. Biological inventory of Ranomafana National Park tetrapods using leech-derived iDNA. European Journal of Wildlife Research 65: 70. <https://doi.org/10.1007/s10344-019-1305-3>

Fahmy, M., Williams, K. M., Tessler, M., Weiskopf, S. R., Hekkala, E. and Siddall, M. E. 2020. Multilocus metabarcoding of terrestrial leech bloodmeal iDNA increases species richness uncovered in surveys of vertebrate host biodiversity. Journal of Parasitology 106, 6: 843–853. <https://doi.org/10.1645/19-189>

Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 5: 294–299. Available online <https://scispace.com/papers/dna-primers-foramplification-of-mitochondrial-cytochrome-c-46m2jyijnx>

Harding, W. A. and Moore, J. P. 1927. The Fauna of British India, including Ceylon and Burma. Hirudinea. Taylor and Francis, Calcutta and Bombay. Available online <https://archive.org/details/dli.csl.8278>

Iyer, R. G., Valle Rogers, D., Levine, M., Winchell, C. J. and Weisblat, D. A., 2019. Reproductive differences among species, and between individuals and cohorts, in the leech genus Helobdella (Lophotrochozoa; Annelida; Clitellata; Hirudinida; Glossiphoniidae), with implications for reproductive resource allocation in hermaphrodites. PLoS ONE 14, 4: e0214581. <https://doi.org/10.1371/journal.pone.0214581>

Kikinis, R., Pieper, S. D., Vosburgh and Vosburgh, K. G. 2014. 3D Slicer: A platform for subject-specific Image analysis, visualization, and clinical support. In: Intraoperative Imaging and Image-Guided Therapy. F. A. Jolesz (ed.), pp 277–289. Springer New York, Heidelberg, Dordrecht, London. <https://doi.org/10.1007/978-1-4614-7657-3_19>

Kutschera, U. and Weisblat, D. A. 2015. Leeches of the genus Helobdella as model organisms for Evo-Devo studies. Theory in Biosciences 134: 93–104. <https://doi.org/10.1007/S12064-015-0216-4>

Lai, Y.-T., Nakano, T. and Chen, J.-H. 2011. Three species of land leeches from Taiwan, Haemadipsa rjukjuana comb. n., a new record for Haemadipsa picta Moore, and an updated description of Tritetrabdella taiwana (Oka). ZooKeys 139: 1–22. <https://doi.org/10.3897/zookeys.139.1711>

Miller, M. A., Pfeiffer, W. and Schwartz, T. 2011. The CIPRES science gateway: a community resource for phylogenetic analyses. In: Proceedings of the 2011 TeraGrid Conference on Extreme Digital Discovery, 2011 Jul 18, pp 1–8. <https://doi.org/10.1145/2016741.2016785>

Morishima, K. and Aizawa, M. 2019. Nuclear microsatellite and mitochondrial DNA analyses reveal the regional genetic structure and phylogeographical history of a sanguivorous land leech, Haemadipsa japonica, in Japan. Ecology and Evolution 9, 9: 5392–5406. <https://doi.org/10.1002/ece3.5132>

Rambaut, A. 2010. FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh. Available online <http://tree.bio.ed.ac.uk/software/figtree/>

Richardson, L. R. 1975. A contribution to the general zoology of the land-leeches (Hirudinea: Haemadipsoidea superfam. nov.). Acta Zoologica Academiae Scientiarum Hungaricae 21, 1–2: 119–152. Available online <https://archive.org/details/actazoologicaacademiaescientiarumhungaricae0021/page/118>

Rocha, R., Borda, E., Andreone, F. and Rosa, G.M. 2012. First reports of leech parasitism in Malagasy Anurans. Comparative Parasitology 79, 2: 352–356. <https://doi.org/10.1654/4546.1>

Schnell, I. B., Thomsen, P. F., Wilkinson, N., Rasmussen, M., Jensen, L. R. D., et al. 2012. Screening mammal biodiversity using DNA from leeches. Current Biology 22, 8: 262–263. <https://doi.org/10.1016/j.cub.2012.02.058>

Schnell, I. B., Bohmann, K., Schultze, S. E., Richter, S .R., Murray, D. C., et al. 2018. Debugging diversity – a pan-continental exploration of the potential of terrestrial blood-feeding leeches as a vertebrate monitoring tool. Molecular Ecology Resources 18, 6: 1282–1298. <https://doi.org/10.1111/1755-0998.12912>

Shafiq-ul-Hassan, M., Zhang, G. G., Latifi, K., Ullah, G., Hunt, D. C., et al. 2017. Intrinsic dependencies of CT radiomic features on voxel size and number of gray levels. Medical Physics 44, 3: 1050–1062. <https://doi.org/10.1002/MP.12123>

Shen, Y.Y., Chen, X. and Murphy, R. W. 2013. Assessing DNA barcoding as a tool for species identification and data quality control. PLoS ONE 8, 2: e57125. <https://doi.org/10.1371/journal.pone.0057125>

Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics 30, 9: 1312–1313. <https://doi.org/10.1093/bioinformatics/btu033>

Tessler, M., Barrio, A., Borda, E., Rood-Goldman, R., Hill, M. and Siddall, M. E. 2016. Description of a soft-bodied invertebrate with microcomputed tomography and revision of the genus Chtonobdella (Hirudinea: Haemadipsidae). Zoologica Scripta 45, 5: 552–565. <https://doi.org/10.1111/zsc.12165>

Tessler, M., Weiskopf, S. R., Berniker, L., Hersch, R., Mccarthy, K. P., et al. 2018. Bloodlines: mammals, leeches, and conservation in southern Asia. Systematics and Biodiversity 16, 5: 488–496. <https://doi.org/10.1080/14772000.2018.1433729>

Wang, H., Meng, F.-M., Jin, S.-J., Gao, J.-W., Tong, X.-R. and Liu, Z.-C. 2022. A new species of medicinal leech in the genus Hirudo Linnaeus, 1758 (Hirudiniformes, Hirudinidae) from Tianjin City, China. Zookeys 1095: 83–96. <https://doi.org/10.3897/ZooKeys.1095.74071>

MuCT scans of diagnostic reproductive anatomy of 3 Malagasy leeches, new species to the right

Downloads

Published

18-07-2025

Issue

Section

Articles