Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5335 No. 1: 18 Aug. 2023
Type: Monograph
Published: 2023-08-18
DOI: 10.11646/zootaxa.5335.1.1
Page range: 1-77
Abstract views: 772
PDF downloaded: 51

Molecular phylogenetics facilitates the first historical biogeographic analysis of the hammerhead worms (Platyhelminthes: Tricladida: Bipaliinae), with the description of twelve new species and two new genera

Departament de Genètica; Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio); Universitat de Barcelona; Barcelona; Catalonia; Spain; Present address: Institut de Biologia Evolutiva; CSIC; Universitat Pompeu Fabra; Barcelona; Catalonia; Spain
Naturalis Biodiversity Center; P.O. Box 9517; 2300 RA Leiden; The Netherlands
Departament de Genètica; Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio); Universitat de Barcelona; Barcelona; Catalonia; Spain
9jō 9chōme 1-8; Shinkotoni; Kita-ku; Sapporo (Hokkaidō) 001-0909; Japan
Platyhelminthes Borneo Bipalium Diversibipalium Humbertium Japan land planarian Novibipalium Madagascar phylogeny Umbotectum Vermiviatum

Abstract

The hammerhead worms constitute a land planarian subfamily (Platyhelminthes: Tricladida: Bipaliinae) that is popular among natural historians as well as citizen scientists due to their characteristic semi-lunar-shaped head, the striking colours of many species, and the worldwide presence of introduced species, which has raised much concern about their putative impact on the receiving ecosystems. Despite such current awareness, the majority of Bipaliinae species was described before the second half of the 20th century. Over the past few decades, description of new species has been rather scarce. In the present paper, we describe twelve new species and two new genera from Madagascar, Borneo, and Japan, mainly using specimens that form part of the collections of Naturalis Biodiversity Center, Leiden. Species identification has been based on morphology, inner anatomy, and, when available, molecular information. Our molecular phylogenetic tree suggests that either Malagasy or Bornean representatives form the sister-group to the rest of Bipaliinae. The phylogeny suggests also that the Bipaliinae comprises several new and, as yet, undescribed genera. Although the geographical origin of the subfamily is uncertain and may involve either Madagascar or the Bornean region, a molecular time-calibration of the phylogenetic tree indicated that the origin of the Bipaliinae may date back to about 253 Mya, placing its origin near the Permian-Triassic transition and, thus, on Pangea.

 

References

  1. Abadi, S., Azouri, D., Pupko, T. & Mayrose, I. (2019) Model selection may not be a mandatory step for phylogeny reconstruction. Nature Communications, 10 (1), 934. https://doi.org/10.1038/s41467-019-08822-w
  2. Aitchison, J.C., Ali, J.R. & Davis, A.M. (2007) When and where did India and Asia collide? Journal of Geophysical Research: Solid Earth, 112 (5), 1–19. https://doi.org/10.1029/2006JB004706
  3. Ali, J.R. & Aitchison, J.C. (2008) Gondwana to Asia: Plate tectonics, paleogeography and the biological connectivity of the Indian sub-continent from the Middle Jurassic through latest Eocene (166-35 Ma). Earth-Science Reviews, 88 (3–4), 145–166. https://doi.org/10.1016/j.earscirev.2008.01.007
  4. Álvarez-Presas, A., Baguñà, J. & Riutort, M. (2008) Molecular phylogeny of land and freshwater planarians (Tricladida, Platyhelminthes): from freshwater to land and back. Molecular Phylogenetics and Evolution, 47 (2), 555–568. https://doi.org/10.1016/j.ympev.2008.01.032
  5. Álvarez-Presas, M. & Riutort, M. (2014) Planarian (Platyhelminthes, Tricladida) diversity and molecular markers: a new view of an old group. Diversity, 6 (2), 323–338. https://doi.org/10.3390/d6020323
  6. Andrey, P. & Maurin, Y. (2005) Free-D: An integrated environment for three-dimensional reconstruction from serial sections. Journal of Neuroscience Methods, 145 (1–2), 233–244. https://doi.org/10.1016/j.jneumeth.2005.01.006
  7. Baguñà, J., Carranza, S., Paps, J., Ruiz-Trillo, I. & Riutort, M. (2001) Molecular taxonomy and phylogeny of the Tricladida. In: Littlewood, D.T.J. & Bray, R.A (Eds.), Interrelationships of the Platyhelminthes. The Systematics Association Special Volume Series 60. Taylor & Francis, London and New York, pp. 49–56. https://doi.org/10.1201/9781482268218
  8. Carranza, S., Giribet, G., Ribera, C., Baguñà, J. & Riutort, M. (1996) Evidence that two types of 18S rDNA coexist in the genome of Dugesia (Schmidtea) mediterranea (Platyhelminthes, Turbellaria, Tricladida). Molecular Biolology and Evolution, 13 (6), 824–832. https://doi.org/10.1093/oxfordjournals.molbev.a025643
  9. de Beauchamp, P. (1919) Diagnoses préliminaires de Triclades obscuricoles. Bulletin de la Société Zoologique de France, 44, 243–251.
  10. de Beauchamp, P. (1926) Planaires terrestres de Sarawak. The Sarawak Museum Journal, 3 (3), 323–358.
  11. de Beauchamp, P. (1930) Turbellariés Triclades de l’Inde méridionale. Revue Suisse de Zoologie, 37 (23), 673–746.
  12. de Beauchamp, P. (1939) Planaires terrestres de l’Indochine française, récoltées par M. C. Dawydoff. Mémoires du Muséum National d’Histoire Naturelle, 10 (6), 299–338.
  13. de Beauchamp, P. (1940) Planaires terrestre du Raffles Museum (deuxième note). Bulletin of the Raffles Museum, 16, 114–118.
  14. de Luna, M., García-Barrios, R., Ovalle, P. & Boll, P.K. (2022) New records of invasive hammerhead flatworms (Platyhelminthes, Geoplanidae, Bipaliinae) from Mexico using a citizen science platform, with an identification key to the species found in North America. Check List, 18 (5), 925–935. https://doi.org/10.15560/18.5.925
  15. Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29 (8), 1969–1973. https://doi.org/10.1093/molbev/mss075
  16. Ducey, P.K., West, L.-J., Shaw, G. & De Lisle, J. (2005) Reproductive ecology and evolution in the invasive terrestrial planarian Bipalium adventitium across North America. Pedobiologia, 49 (4), 367–377. https://doi.org/10.1016/j.pedobi.2005.04.002
  17. Ducey, P.K., McCormick, M. & Davidson, E. (2007) Natural history observations on Bipalium cf. vagum Jones and Sterrer, 2005 (Platyhelminthes: Tricladida), a terrestrial broadhead planarian new to North America. Southeastern Naturalist, 6 (3), 449–460. [http://www.jstor.org/stable/4541040]
  18. Fourcade, Y., Winsor, L. & Justine, J.-L. (2022) Hammerhead worms everywhere? Modelling the invasion of bipaliin flatworms in a changing climate. Diversity and Distributions, 28, 844–858. https://doi.org/10.1111/ddi.13489
  19. Grube, E. (1866). Beschreibungen neuer von der Novara-Expedition mitgebrachter Anneliden und einer neuen Landplanarie. Verhandlugen der Kaiserligh-Königlichen Zoologisch-Botanischen Gesellschaft in Wien, 16, 173–184.
  20. Humason, G.L. (1967) Animal tissue techniques. W. H. Freeman and Company, San Francisco and London, 569 pp.
  21. Hyman, L.H. (1943) Endemic and exotic land planarians in the United States with a discussion of necessary changes of names in the Rhynchodemidae. American Museum Novitates, 1241, 1–21.
  22. Jones, H.D., Johns, P.M. & Winsor, L. (1998) The proposed synonymy of Parakontikia ventrolineata (Dendy, 1892) and Kontikia mexicana (Hyman, 1939): what is a penis papilla? Hydrobiologia, 383, 91–96. https://doi.org/10.1023/A:1003478218873
  23. Justine, J.-L., Winsor, L., Gey, D., Gros, P. & Thévenot, J. (2018) Giant worms chez moi! Hammerhead flatworms (Platyhelminthes, Geoplanidae, Bipalium spp., Diversibipalium spp.) in metropolitan France and overseas French territories. PeerJ, 6, e4672 https://doi.org/10.7717/peerj.4672
  24. Justine, J.-L., Gastineau, R., Gros, P., Gey, D., Ruzzier, E., Charles, L. & Winsor, L. (2022) Hammerhead flatworms (Platyhelminthes, Geoplanidae, Bipaliinae): mitochondrial genomes and description of two new species from France, Italy, and Mayotte. PeerJ, 10, e12725 https://doi.org/10.7717/peerj.12725
  25. Kaburaki, T. (1922) On the terrestrial planarians from Japanese territories. Journal of the College of Science, Tokyo Imperial University, 44, 1−54, pl. I.
  26. Katoh, K. & Standley, D.M. (2013) MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Molecular Biology and Evolution, 30 (4), 772−780. https://doi.org/10.1093/molbev/mst010
  27. Kawakatsu, M., Makino, N. & Shirasawa, Y. (1982) Bipalium nobile sp. nov. (Turbellaria, Tricladida, Terricola), a new land planarian from Tokyo. Annotationes Zoologicae Japonenses, 55 (4), 236–262.
  28. Kawakatsu, M., Ogren, R.E. & Froehlich, E.M. (1998) The taxonomic revision of several homonyms in the genus Bipalium, family Bipaliidae (Turbellaria, Seriata, Tricladida, Terricola). The Bulletin of Fuji Women’s College, No. 36, Series II, 36, 83–93.
  29. Kawakatsu, M., Ogren, R.E. & Froehlich E.M. (2001) On the places of origin of three, very large bipaliid land planarians from Japan (Turbellaria, Seriata, Tricladida, Terricola). Shibukitsubo, 22, 39–52.
  30. Kawakatsu, M., Ogren, R.E., Froehlich, E.M. & Sasaki, G.Y. (2002) Additions and corrections of the previous land planarian indices of the world (Turbellaria, Seriata, Tricladida, Terricola)—10. The Bulletin of Fuji Women’s University, No. 40, Series II, 40, 162–177.
  31. Kawakatsu, M., Sluys, R. & Ogren R.E. (2005) Seven new species of land planarian from Japan and China (Platyhelminthes, Tricladida, Bipaliidae), with a morphological review of all Japanese bipaliids and a biogeographic overview of Far Eastern species. Belgian Journal of Zoology, 135 (1), 53–77.
  32. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
  33. Mazza, G., Menchetti, M., Sluys, R., Solà, E., Riutort, M., Tricarico, E., Justine, J.-L., Cavigioli, L. & Mori, E. (2016) First report of the land planarian Diversibipalium multilineatum (Makino & Shirasawa, 1983) (Platyhelminthes, Tricladida, Continenticola) in Europe. Zootaxa, 4067 (5), 577–80. https://doi.org/ 10.11646/zootaxa.4067.5.4
  34. Morffe, J., García, N., Adams, B.J. & Hasegawa, K. (2016) First record of the land planarian Bipalium kewense Moseley, 1878 (Tricladida: Geoplanidae; Bipaliinae) from Cuba. BioInvasions Records, 5 (3), 127–132. https://doi.org/10.3391/bir.2016.5.3.01
  35. Morgan, T.H. (1900) Regeneration in Bipalium. Archiv für Entwicklungsmechanik der Organismen, 9 (4), 563–586.
  36. Mori, E., Magoga, G., Panella, M., Montagna, M., Winsor, L., Justine, J.-L., Menchetti, M., Schifani, E., Melone, B. & Mazza, G. (2022) Discovering the Pandora’s box: the invasion of alien flatworms in Italy. Biological Invasions, 24, 205–216. https://doi.org/10.1007/s10530-021-02638-w
  37. Müller, J. (1902) Ein Beitrag zur Kenntnis der Bipaliiden. Zeitschrift für wissenschaftliche Zoologie, 73, 75–114.
  38. Müller, J. (1907) Weitere Beiträge zur Kenntnis der Bipaliiden. Zeitschrift für wissenschaftliche Zoologie, 86, 416–445.
  39. Ogren, R.E. (1987) Description of a new three-lined planarian of the genus Bipalium (Turbellaria: Tricladida) from Pennsylvania, U.S.A. Transactions of the American Microscopical Society, 106 (1), 21–30. https://doi.org/10.2307/3226281
  40. Ogren, R.E., Kawakatsu, M. & Froehlich, E. (1992) Additions and corrections of the previous land planarian indices of the world (Turbellaria, Tricladida, Terricola). The Bulletin of Fuji Women’s College, Series II, No. 30, 3, 59–103.
  41. Ogren, R.E. & Sluys, R. (2001) The genus Humbertium gen. nov., a new taxon of the land planarian family Bipaliidae (Tricladida, Terricola). Belgian Journal of Zoology, 131 (Supplement 1), 201–204.
  42. Patra, B.C. & Aditya, A.K. (2001) Circular form of regeneration in an unidentified species of land planarians, Bipalium sp. Indian Journal of Experimental Biology, 39 (5), 496–499.
  43. Prozorova, L.A. (2021) New findings of hammerhead planarians (Platyhelminthes: Tricladida: Continenticola: Bipaliinae) on the Russian Far East. Biota and Environment of Natural Areas, 1, 55–64. [in Russian]
  44. Prozorova, L.A. & Ternovenko, V.A. (2018) Rare and new species from the Far Eastern Marine Reserve. 2. Land Planarians (Platyhelminthes: Tricladida: Continenticola). Biota and Environment, 3, 54–59. [in Russian]
  45. Rabinowitz, P.D. & Woods, S. (2006) The Africa-Madagascar connection and mammalian migrations. Journal of African Earth Science, 44 (3), 270–276. https://doi.org/10.1016/j.jafrearsci.2005.12.005
  46. Ronquist, F., Teslenko, M., Mark, P.V.D., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic Biology, 61 (3), 539–542. https://doi.org/10.1093/sysbio/sys029
  47. Schettino, A. & Scotese, C.R. (2005) Apparent polar wander paths for the major continents (200 Ma to the present day): a palaeomagnetic reference frame for global plate tectonic reconstructions. Geophysical Journal International, 163 (2), 727–759. https://doi.org/10.1111/j.1365-246X.2005.02638.x
  48. Shirasawa, Y. & Makino, N. (1991) Pharyngeal regeneration in the land planarian Bipalium kewense. Hydrobiologia, 227, 57. https://doi.org/10.1007/BF00027581
  49. Sluys, R. (2016) Invasion of the flatworms. American Scientist, 104, 288–295.
  50. Sluys, R., Kawakatsu, M., Riutort, M. & Baguñà, J. (2009) A new higher classification of planarian flatworms (Platyhelminthes, Tricladida). Journal of Natural History, 43 (29–30), 1763–1777. https://doi.org/10.1080/00222930902741669
  51. Sluys, R., Neumann, M., Lima, R.F. & Drewes, R.C. (2017) Land flatworms (Platyhelminthes, Geoplanidae) of São Tomé: a first account on their diversity, with the description of five new species. Zootaxa, 4221 (3), 291–322. https://doi.org/10.11646/zootaxa.4221.3.2
  52. Sluys, R. & Riutort, M. (2018) Planarian diversity and phylogeny. In: Rink, J.C. (Ed.), Planarian Regeneration: Methods and Protocols. Methods in Molecular Biology, Vol. 1774. Humana Press, Springer Science+Business Media, New York, New York, pp. 1–56.
  53. Solà, E., Leria, L., Stocchino, G.A., Bagherzadeh, R., Balke, M., Daniels, S.R., Harrath, A.H., Khang, T.F., Krailas, D., Kumar, B., Li, M.-H., Maghsoudlou, A., Matsumoto, M., Naser, N., Oben, B., Segev, O., Thielicke, M., Tong, X., Zivanovic, G., Manconi, R., Baguñà, J. & Riutort, M. (2022) Three dispersal routes out of Africa: A puzzling biogeographical history in freshwater planarians. Journal of Biogeography, 49, 1219–1233. https://doi.org/10.1111/jbi.14371
  54. Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30 (9), 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
  55. Stimpson, W. (1857) Prodromus descriptionis animalium evertebratorum, quae in Expeditione ad Oceanum, Pacificum Spetentionalem a Republica Federata missa, Johanne Rodgers Duce, observavit et descripsit. Pars. I. Turbellaria Dendrocoela. Proceedings of the Academy of Natural Sciences of Philadelphia, 9, 19–31.
  56. Stokes, A.N., Ducey, P.K., Lorin, N.-L., Hanifin, C.T., French, S.S., Pfrender, M.E., Brodie III, E.D. & Brodie, E.D. Jr. (2014) Confirmation and distribution of tetrodotoxin for the first time in terrestrial invertebrates: two terrestrial flatworm species (Bipalium adventitium and Bipalium kewense). PLoS ONE, 9 (6), e100718. https://doi.org/10.1371/journal.pone.0100718
  57. Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology, 56 (4), 564–577. https://doi.org/10.1080/10635150701472164
  58. Yamamoto, K., Takai, M., Ogren, R.E. & Kawakatsu M. (2001) Chromosomes of bipaliid land planarians from the vicinity of Nagasaki in Kyūshū, southern Japan (Platyhelminthes, Tricladida, Terricola). Belgian Journal of Zoology, 131 (Supplement 1), 221–222.
  59. Yamamoto, K., Kawakatsu, M. & Sasaki G. (2003) Bipaliid land planarians from Nagasaki Prefecture and the vicinity, Kyūshū, Japan: color photographs of living specimens and the karyotypes. Kawakatsu & Sasaki’s webpages on planarians, Sapporo and Tōkyō, 40, 1–9. Available from: http://planarian.net/kswp/40/nagasaki.pdf/ (accessed 3 April 2022)
  60. van Hinsbergen, D.J., Lippert, P.C., Dupont-Nivet, G., McQuarrie, N., Doubrovine, P.V., Spakman, W. & Torsvik, T.H. (2012) Greater India Basin hypothesis and a two-stage Cenozoic collision between India and Asia. Proceedings of the National Academy of Science of the United States of America, 109 (20), 7659–7664. https://doi.org/10.1073/pnas.1117262109
  61. von Graff, L. (1896) Über das System und die geographische Verbreitung der Landplanarien. Verhandlungen der Deutschen Zoologischen Gesellschaft, 6, 75–93.
  62. von Graff, L. (1899) Monographie der Turbellarien. II. Tricladida Terricola (Landplanarien). Atlas von Achtundfünfzig Tafeln zur Monographie der Turbellarien II. Tricladida Terricola (Landplanarien). Wilhelm Engelmann, Leipzig, XII + 574 pp., pls. I–LVIII.
  63. Ward, P., Labandeira, C., Laurin, M. & Berner, R.A. (2006) Confirmation of Romer’s Gap as a low oxygen interval constraining the timing of initial arthropod and vertebrate terrestrialization. Proceedings of the National Academy of Sciences, 103 (45), 16818–16822. https://doi.org/10.1073/pnas.0607824103
  64. Winsor, L. (1983) A revision of the cosmopolitan land planarian Bipalium kewense Moseley, 1878 (Turbellaria: Tricladida: Terricola). Zoological Journal of the Linnean Society, 79 (1), 61–100. https://doi.org/10.1111/j.1096-3642.1983.tb01161.x
  65. Winsor, L. (1998) Aspects of taxonomy and functional histology in terrestrial flatworms (Tricladida: Terricola). Pedobiologia, 42, 412–432.
  66. Winsor, L., Johns, P.M. & Barker, G.M. (2004) Terrestrial planarians (Platyhelminthes: Tricladida: Terricola) predaceous on terrestrial gastropods. In: Barker, G.M. (Ed.), Natural enemies of terrestrial molluscs. CAB International, Oxfordshire, pp. 227–278. https://doi.org/10.1079/9780851993195.0227
  67. Winsor, L. & Sluys, R. (2018) Basic histological techniques for planarians. In: Rink, J. (Ed.), Planarian regeneration: Methods and Protocols. Methods in Molecular Biology, Vol. 1774. Humana Press, Springer Science+Business Media, New York, New York, pp. 285–351. https://doi.org/10.1007/978-1-4939-7802-1_9