Advertisement

Marine gastrotrichs from Lanzarote, with a description of a phylogenetically relevant species of Urodasys (Gastrotricha, Macrodasyida)

  • M. Antonio TodaroEmail author
  • Agata Cesaretti
  • Matteo Dal Zotto
MeioLanza
Part of the following topical collections:
  1. Interstitial and Cave Diversity in Atlantic Oceanic Islands

Abstract

Sampling campaign took place in October 2011 and included 7 locations and 16 stations along the eastern coast of the island of Lanzarote (Spain). Samples yielded 61 species for a total of 96 records. Thirty-six species (27 genera and 11 families) belong to Macrodasyida while 25 species (18 genera, 7 families) to Chaetonotida. Thirty-two are known species while 29 appear to be undescribed taxa or putatively so. The finding at Lanzarote of some of the known species bear particular significance: Oregodasys cirratus and Tetranchyroderma canariense are recorded for the second time ever, while Musellifer delamarei and Urodasys acanthostylis were previously known only from the Mediterranean, and Urodadys mirabilis was acknowledged only for northern Europe. Furthermore, the presence of Chaetonotus apechochaetus, C. apolemmus, C. siciliensis, Heterolepidoderma loricatum, Lepidodasys unicarenatus, Musellifer delamarei, Thaumastoderma mediterraneum, and Urodasys acanthostylis strongly suggest them to be part of the temperate/warm fauna that invaded the Mediterranean basin after the Missinian crisis during the different climate eras. Of the new species, one is described as its characteristics substantially widen our knowledge of the entire genus. Urodasys completus sp. nov. is unique in that it possesses, among others, two testes and a sclerotic stylet. Results of a phylogenetic analysis indicated that the sequence of the evolutionary transformation that have occurred in the reproductive system of the species of Urodasys are likely dissimilar from the ones proposed thus far. The overall results testify the need to continue the exploration in the Canary Islands.

Keywords

Meiofauna Benthos Spanish biodiversity Canary islands Phylogeny Taxonomy 

Notes

Acknowledgements

Many thanks to the colleagues and students who made extremely enjoyable the stay on the Island. Special appreciations go to the chief collectors: Marco Curini Galletti, Alejandro Martínez, Maikon Di Domenico and Tom Artois. The senior author expresses sincere gratitude to Katrine Worsaae and Alejandro Martínez who invited him to the workshop, which was superbly organized. Additional funding was provided by UNIMORE (TIOME project) to MA Todaro. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Finally, we thank two anonymous reviewers for their insightful comments.

References

  1. Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T, Bailly N et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202Google Scholar
  2. Araujo TQ, Atherton S, Hochberg R (2015) First record and a description of a new species of Oregodasys (Gastrotricha: Macrodasyida: Thaumastodermatidae) from Tobago. Proc Biol Soc Wash 128:176–185Google Scholar
  3. Araujo TQ, Balsamo M, Garraffoni ARS (2014) A new species of Pseudostomella (Gastrotricha, Thaumastodermatidae) from Brazil. Mar Biodiv 44:243–248Google Scholar
  4. Artois T, Fontaneto D, Hummon WD, McInnes SJ, Todaro MA, Sørensen MV, Zullini A (2011) Ubiquity of microscopic animals? Evidence from the morphological approach in species identification. In: Fontaneto D (ed) Biogeography of microscopic organisms: is everything small everywhere? Cambridge University Press, Cambridge, pp 244–283Google Scholar
  5. Atherton S (2014) Urodasys poculostylis sp. nov., a new stylet-bearing gastrotrich (Macrodasyida) from Capron shoal, Florida. Mar Biol Res 5:530–536Google Scholar
  6. Atherton S, Hochberg R (2014) The evolution of the reproductive system of Urodasys (Gastrotricha: Macrodasyida). Invert Biol 133:314–323Google Scholar
  7. Balsamo M, Todaro MA (2002) Gastrotricha. In: Rundle SD, Robertson AL, Schmid-Araya JM (eds) Freshwater Meiofauna: Biology and Ecology. Backhuys, Leiden, pp 45–61Google Scholar
  8. Buchanan JB (1984) Sediment analysis. In: Holme NA, McIntyre AD (eds) Methods for the study the marine benthos, vol 16. Blackwell, London, pp 41–65Google Scholar
  9. Camargo MG (2006) Sysgran: um sistema de codigo aberto para analises granulometricas do sedimento. Rev Bras Geosci 345:345–352Google Scholar
  10. Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F, Aguzzi J, Ballesteros E, Bianchi CN, Corbera J, Dailianis T, Danovaro R, Estrada M, Froglia C, Galil BS, Gasol JM, Gertwagen R, Gil J, Guilhaumon F, Kesner-Reyes K, Kitsos MS, Koukouras A, Lampadariou N, Laxamana E, Carlos M, de la Cuadra L, Lotze HK, Martin D, Mouillot D, Oro D, Raicevich S, Rius-Barile J, Saiz-Salinas JI, San Vicente C, Somot S, Templado J, Turon X, Vafidis D, Villanueva R, Voultsiadou E (2010) The biodiversity of the Mediterranean Sea: estimates, Patterns, and threats. PLoS ONE 5(8):e11842PubMedPubMedCentralGoogle Scholar
  11. Coull BC (1985) Long-term variability of estuarine meiobenthos: an 11 year study. Mar Ecol Prog Ser 24:205–218Google Scholar
  12. Curini-Galletti M, Artois T, Delogu V, De Smet WH, Fontaneto D, Jondelius U, Leasi F, Martinez A, Meyer-Wachsmuth I, Nilsson KS, Tongiorgi P, Worsaae K, Todaro MA (2012) Patterns of diversity in soft-bodied Meiofauna: dispersal ability and Body size matter. PLoS ONE 7(3):e33801PubMedPubMedCentralGoogle Scholar
  13. Dal Zotto M, Ghiviriga S, Todaro MA (2010) A new Tetranchyroderma (Gastrotricha, Thaumastodermatidae) with triancres from the Mediterranean Sea. Meiofauna Mar 18:41–48Google Scholar
  14. Dewarumez JM, d’Hondt JL, Hummon WD (2002) Faune et Flore du littoral du Pas de Calais et de la manche orientale. Mise àjour de la liste des espèces de Gastrotriches et de Céphalorhynques. Rev Trav Stat Mar Wimereux 24:7–9Google Scholar
  15. Egger B, Lapraz F, Müller S, Dessimoz C, Girstmair J, Skunca N, Rawlinson KA, Cameron CB, Beli E, Todaro MA, Gammoudi M, Noreña C, Telford MJ (2015) A transcriptomic-Phylogenomic analysis of the evolutionary relationships of flatworms. Curr Biol 25:1–7Google Scholar
  16. Fregni E, Tongiorgi P, Faienza MG (1998) Two new species of Urodasys (Gastrotricha, Macrodasyidae) with cuticular stylet. Ital J Zool 65:377–380Google Scholar
  17. Fregni E, Faienza MG, Grimaldi-De Zio S, Tongiorgi P, Balsamo M (1999) Marine gastrotrichs from the Tremiti archipelago in the southern Adriatic Sea, with the description of two new species of Urodasys. Ital J Zool 66:183–194Google Scholar
  18. Garraffoni ARS, Di Domenico M, Amaral ACZ (2016a) Patterns of diversity in marine Gastrotricha from southeastern Brazilian coast is predicted by sediment textures. Hydrobiologia 773:105–116Google Scholar
  19. Garraffoni ARS, Di Domenico M, Hochberg R (2016b) New records of marine Gastrotricha from São Sebastião Island (Brazil) and the description of a new species. Mar Biodivers. doi: 10.1007/s12526-016-0486-1 Google Scholar
  20. Giere O (1979) The impact of oil pollution on intertidal meiofauna. Field studies after the la Coruña-spill, may 1976. Cah Biol Mar 20:231–251Google Scholar
  21. Gray JS (1971) The effects of pollution on sand meiofauna communities. In: Zavodnik D (ed) Proceedings of the Sixth European Symposium on Marine Biology, Rovinj, Croatia, Yugoslavia, September 27–October 2, 1971. Thalass Jugosl 7:79–86Google Scholar
  22. Guidi L, Todaro MA, Ferraguti M, Balsamo M (2014) Reproductive system and spermatozoa ultrastructure support the phylogenetic proximity of Megadasys and Crasiella (Gastrotricha, Macrodasyida). Contr Zool 83:119–131Google Scholar
  23. Hochberg R (1999) Spatiotemporal size-class distribution of Turbanella mustela (Gastrotricha: Macrodasyida) on a northern California beach and its effect on tidal suspension. Pacific Sci 53:50–60Google Scholar
  24. Hochberg R (2014) Crasiella fonseci, a new species of Gastrotricha (Macrodasyida, Planodasyidae) from São Paulo, Brazil. Mar Biodivers 44:237–242Google Scholar
  25. Hochberg R, Atherton S, Kieneke A (2014) Marine Gastrotricha of little Cayman Island with the description of one new species and an initial assessment of meiofaunal diversity. Mar Biodivers 44:89–113Google Scholar
  26. Hsü KJ (1983) The Mediterranean was a desert. Princeton University Press, PrincetonGoogle Scholar
  27. Hummon WD (1969) Musellifer sublitoralis, a new genus and species of Gastrotricha from the San Juan archipelago, Washington. Trans Am Microsc Soc 88:282–286Google Scholar
  28. Hummon WD (2008) Gastrotricha of the North Atlantic Ocean: 1. Twenty four new and two redescribed species of Macrodasyida. Meiofauna Mar 16:117–174Google Scholar
  29. Hummon WD (2010a) Marine Gastrotricha of San Juan Island, Washington, USA, with notes on some species from Oregon and California. Meiofauna Mar 18:11–40Google Scholar
  30. Hummon WD (2010b) Marine Gastrotricha of the Caribbean Sea: a review and new descriptions. Bull Mar Sci 86:661–708Google Scholar
  31. Hummon WD (2011) Marine Gastrotricha of the near east: 1. Fourteen new species of Macrodasyida and a redescription of Dactylopodola agadasys Hochberg, 2003. Zookeys 94:1–59Google Scholar
  32. Hummon WD, Roidou E (1995) Marine Gastrotricha of Greece: a preliminary report. Biol Gallo-Hellen 22:279–289Google Scholar
  33. Hummon WD, Todaro MA (2009) Italian marine Gastrotricha: VI. Seven New Species Macrodasyida. Zootaxa 2278:47–68Google Scholar
  34. Hummon WD, Todaro MA (2010) Analytic taxonomy and notes on marine, brackish-water and estuarine Gastrotricha. Zootaxa 2392:1–32Google Scholar
  35. Hummon WD, Warwick RM (1990) The marine flora and fauna of the isles of Scilly - Gastrotricha. J Nat Hist 24:519–525Google Scholar
  36. Hummon WD, Balsamo M, Todaro MA (1992) Italian marine Gastrotricha: I. Six new and one redescribed species of Chaetonotida. Boll Zool 59:499–516Google Scholar
  37. Hummon WD, Todaro MA, Tongiorgi P (1993) Italian marine Gastrotricha: II. One new genus and ten new species of Macrodasyida. Boll Zool 60:109–127Google Scholar
  38. Hummon WD, Todaro MA, Kånneby T, Hochberg R (2010) Marine Gastrotricha of the Caribbean Sea. Proc. 14th International Meiofauna Conference, GentGoogle Scholar
  39. Jouk PEH, Hummon WD, Hummon MR, Roidou E (1992) Marine Gastrotricha from the Belgian coast: species list and distribution. Bull Inst R Sci Nat 62:87–93Google Scholar
  40. Kånneby T, Todaro MA (2015) The phylogenetic position of Neogosseidae (Gastrotricha:Chaetonotida) and the origin of planktonic Gastrotricha. Org Div Evol 15:459–469Google Scholar
  41. Kånneby T, Atherton S, Hochberg R (2014) Two new species of Musellifer (Gastrotricha: Chaetonotida) from Florida and Tobago and the systematic placement of the genus within Paucitubulatina. Mar Biol Res 10:983–995Google Scholar
  42. ,Kieneke A, Schmidt-Rhaesa A (2014) Gastrotricha. In: Schmidt-Rhaesa A (ed) Handbook of zoology. Vol.3, Gastrotricha and Gnathifera. De Gruyter, BerlinnGoogle Scholar
  43. Kieneke A, Martinez Arbizu P, Fontaneto D (2012) Spatially structured populations with a low level of cryptic diversity in European marine Gastrotricha. Mol Ecol 21:1239–1254Google Scholar
  44. Kieneke A, Rothe BH, Schmidt-Rhaesa A (2013a) Record and description of Anandrodasys agadasys (Gastrotricha:Redudasyidae) from lee Stocking Island (Bahamas), with remarks on populations from different geographic areas. Meiofauna Mar 20:39–48Google Scholar
  45. Kieneke A, Narkus S, Hochberg R, Schmidt-Rhaesa A (2013b) Diplodasys rothei n. Sp. (Gastrotricha, Macrodasyida), a new marine gastrotrich species from the Bahamas. Meiofauna Mar 20:49–61Google Scholar
  46. Kieneke A, Schmidt-Rhaesa A, Hochberg R (2015) A new species of Cephalodasys (Gastrotricha, Macrodasyida) from the Caribbean Sea with a determination key to species of the genus. Zootaxa 3947:367–385Google Scholar
  47. Kolicka M, Kisielewski J, Kotwicki L, Zawierucha K, Grzelak K (2014) Checklist of Gastrotricha of the polish Baltic Sea with the first reports of Heterolepidoderma joermungandri Kånneby, 2011, and Turbanella hyalina Schultze, 1853. Zootaxa 3869:101–130Google Scholar
  48. Kolicka M, Jankowska E, Kotwicki L (2015) Baltic Sea Gastrotricha-one new species and one new record of Chaetonotida from Poland. Zootaxa 4027:487–508Google Scholar
  49. Leasi F, Todaro MA (2009) Meiofaunal cryptic species revealed by confocal microscopy: the case of Xenotrichula intermedia (Gastrotricha). Mar Biol 156:1335–1346Google Scholar
  50. Leasi F, Todaro MA (2010) The gastrotrich community of a north Adriatic Sea site, with a redescription of Musellifer profundus (Chaetonotida: Muselliferidae). J Mar Biol Assoc UK 90:645–653Google Scholar
  51. Marina P, Rueda JL, Urral J, Salas C, Gofas S, García Raso JE, Moya F, García T, Lóopez-González N, Laiz-Carrión BJ (2015) Sublittoral soft bottom assemblages within a marine protected area of the northern Alboran Sea. J Mar Biol Assoc U K 95:871–884Google Scholar
  52. Marotta R, Todaro MA, Ferraguti M (2008) The unique gravireceptor organs of Pleurodasys helgolandicus (Gastrotricha: Macrodasyida). Zoomorphology 127:111–119Google Scholar
  53. McCammon RB (1962) Efficiencies of percentile measures for describing the mean size and sorting of sedimentary particles. J Geol 70:453–465Google Scholar
  54. Remane A (1927) Gastrotricha. In: Grimpe G (ed) Die Tierwelt der Nord- und Ostsee. Akademische Verlag, LeipzigGoogle Scholar
  55. Riera R, Todaro MA (2012) Check list of gastrotrichs from the Canary Islands. Rev Acad Canar Cienc 24:81–88Google Scholar
  56. Rothe BH, Schmidt-Rhaesa A (2010) Oregodasys cirratus, a new species of Gastrotricha (Macrodasyida) from Tenerife (Canary Islands), with a description of the muscular and nervous system. Meiofauna Mar 18:49–66Google Scholar
  57. Schuster J, Atherton S, Todaro MA, Schmidt-Rhaesa A, Hochberg R (2017) Redescription of Xenodasys riedli (Gastrotricha:Macrodasyida) based on SEM analysis, with first report of population density data. Mar Biodivers. doi: 10.1007/s12526-017-0667-6 Google Scholar
  58. Struck TH, Wey-Fabrizius AR, Golombek A et al (2014) Platyzoan paraphyly based on phylogenomic data supports a noncoelomate ancestry of Spiralia. Mol Biol Evol 31:1833–1849Google Scholar
  59. Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer, SunderlandGoogle Scholar
  60. Todaro MA (1998) Meiofauna from the Meloria shoals: Gastrotricha, biodiversity and seasonal dynamics. Biol Mar Medit 5:587–590Google Scholar
  61. Todaro MA (2012) A new marine gastrotrich from the State of São Paulo (Brazil), with a key to species of Pseudostomella (Gastrotricha, Thaumastodermatidae). ZooKeys 223:39–51Google Scholar
  62. Todaro MA (2013) A new non-naked species of Ptychostomella (Gastrotricha) from Brazil. Zookeys 289:13–24Google Scholar
  63. Todaro MA (2017) Marine. In: Todaro MA (ed) Gastrotricha World Portal. “http://www.gastrotricha.unimore.it/marine.htm” Accessed on 14 February 2017
  64. Todaro MA, Leasi F (2013) A new eye-bearing Macrodasys (Gastrotricha:Macrodasyida) from Jamaica. Meiofauna Mar 20:33–38Google Scholar
  65. Todaro MA, Rocha CEF (2004) Diversity and distribution of marine Gastrotricha along the northern beaches of the state of São Paulo (Brazil), with a description of Macrodasys fornerisae sp. nov. (Macrodasyida, Macrodasyidae). J Nat Hist 38:1605–1634Google Scholar
  66. Todaro MA, Tongiorgi P (2017) Freshwater. In: Todaro MA (ed) Gastrotricha World Portal. http://www.gastrotricha.unimore.it/freshwater.htm. Accessed on 14 February 2017
  67. Todaro MA, Balsamo M, Tongiorgi P (2008) Gastrotricha. In: G Relini (ed) Checklist della flora e della fauna dei mari italiani. Biol Mar Medit 15(suppl.):159–168Google Scholar
  68. Todaro MA, Fleeger JW, Hummon WD (1995) Marine gastrotrichs from the sand beaches of the northern Gulf of Mexico:species list and distribution. Hydrobiologia 310:107–117Google Scholar
  69. Todaro MA, Ancona P, Marzano A, Gallo D’Addabbo M, De Zio GS (2003a) A new Tetranchyroderma species (Gastrotricha, Macrodasyida, Thaumastodermatidae) from the Canary Islands (Spain). Cah Biol Mar 44:191–197Google Scholar
  70. Todaro MA, Matinato L, Balsamo M, Tongiorgi P (2003b) Faunistics and zoogeographical overview of the Mediterranean and Black Sea marine Gastrotricha. Biogeographia 24:131–160Google Scholar
  71. Todaro MA, Kånneby T, Jondelius U (2010) Marine Gastrotricha from Sweden. Proc. 14th International Meiofauna Conference, GentGoogle Scholar
  72. Todaro MA, Dal Zotto M, Perissinotto R, Bownes SJ (2011) First records of Gastrotricha from South Africa, with description of a new species of Halichaetonotus (Chaetonotida, Chaetonotidae). Zookeys 142:1–13Google Scholar
  73. Todaro MA, Perissinotto R, Bownes SJ (2013) Neogosseidae (Gastrotricha, Chaetonotida) from the iSimangaliso Wetland Park, KwaZulu-Natal, South Africa. Zookeys 315:77–94Google Scholar
  74. Todaro MA, Leasi F, Hochberg R (2014) A new species, genus and family of marine Gastrotricha from Jamaica, with a phylogenetic analysis of Macrodasyida based on molecular data. Syst Biodivers 12:473–488Google Scholar
  75. Todaro MA, Perissinotto R, Bownes SJ (2015a) Two new marine Gastrotricha from the Indian Ocean coast of South Africa. Zootaxa 3905:193–208Google Scholar
  76. Todaro MA, Dal Zotto M, Leasi F (2015b) An integrated morphological and molecular approach to the description and systematisation of a novel genus and species of Macrodasyida (Gastrotricha). PLoS ONE 10(7):e0130278PubMedPubMedCentralGoogle Scholar
  77. Wentworth CK (1922) A scale of grade and class terms for clastic sediments. J Geol 30:377–392Google Scholar
  78. Willems WR, Curini-Galletti MC, Ferrero TJ, Fontaneto D, Heiner I, Huys R, Ivanenko VN, Kristensen RM, Kånneby T, MacNaughton MO, Martínez Arbizu P, Todaro MA, Sterrer W, Jondelius U (2009) Meiofauna of the Koster-area, results from a workshop at the Sven Lovén Centre for Marine Sciences (Tjärnö, Sweden). Meiofauna Mar 17:1–34Google Scholar
  79. WoRMS (2017) Statistics in: World Register of Marine Species. http://www.marinespecies.org/aphia.php?p=stats. Accessed 01 March 2017

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of Life SciencesUniversity of Modena and ReggioModenaItaly
  2. 2.Consortium for the Interuniversity Center of Marine Biology and Applied EcologyLivornoItaly

Personalised recommendations