Macrobiotus polypiformis sp. nov., a new tardigrade (Macrobiotidae; hufelandi group) from the Ecuadorian Pacific coast, with remarks on the claw abnormalities in eutardigrades

Milena Roszkowska, Marta Ostrowska, Daniel Stec, Karel Janko, Łukasz Kaczmarek

Abstract


From a moss sample collected in the Manabí Province in Ecuador, we extracted 96 specimens of a new species of eutardigrade. No eggs were found. In order to obtain eggs, an in vitro culture was prepared. In total, 136 specimens (including ten simplex), one exuvia and 44 eggs (including two with embryos) of the new species were obtained. In addition to the traditional taxonomic description with morphometrics, light and scanning microscopy imaging, we also provide nucleotide sequences of three nuclear (18S rRNA, 28S rRNA, ITS-2) and one mitochondrial (COI) DNA fragments of the new species. Macrobiotus polypiformis sp. nov. belongs to the hufelandi group and is most similar to Ma. paulinae Stec, Smolak, Kaczmarek & Michalczyk, 2015, but differs from it mainly by the lack of dorso-lateral patches of granulation on the cuticle, egg processes with longer and more numerous filaments and in some morphometric characters of both eggs and adults. Moreover, we provide a short discussion on the modifications/abnormalities of the claws in eutardigrades and the possible consequences on the taxonomic status of Mesobiotus armatus (Pilato & Binda, 1996), suggesting its consideration as species inquirenda (with uncertain taxonomic status).

Keywords


DNA barcoding; Eutardigrada; new species; Neotropic; water bears

Full Text:

PDF PDF/A


DOI: https://doi.org/10.5852/ejt.2017.327

References


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

Bąkowski M., Roszkowska M., Gawlak M. & Kaczmarek Ł. 2016. Macrobiotus naskreckii sp. nov. (Eutardigrada: Macrobiotidae: hufelandi group) from Mozambique. Annales Zoologici 66 (2): 155–164.

Bertolani R. & Rebecchi L. 1993. A revision of the Macrobiotus hufelandi group (Tardigrada, Macrobiotidae), with some observations on the taxonomic characters of eutardigrades. Zoologica Scripta 22: 127–152. https://doi.org/10.1111/j.1463-6409.1993.tb00347.x

Bertolani R., Biserov V.I., Rebecchi L. & Cesari M. 2011. Taxonomy and biogeography of tardigrades using an integrated approach: new results on species of the Macrobiotus hufelandi group. Invertebrate Zoology 8 (1): 23–36.

Bertolani R., Guidetti R., Marchioro T., Altiero T., Rebecchi L. & Cesari M. 2014. Phylogeny of Eutardigrada: New molecular data and their morphological support lead to the identification of new evolutionary lineages. Molecular Phylogenetics and Evolution 76: 110–126. https://doi.org/10.1016/j.ympev.2014.03.006

Casquet J., Thebaud C. & Gillespie R.G. 2012. Chelex without boiling, a rapid and easy technique to obtain stable amplifiable DNA from small amounts of ethanol-stored spiders. Molecular Ecology Resources 12: 136–141. https://doi.org/10.1111/j.1755-0998.2011.03073.x

Cesari M., Bertolani R., Rebecchi L. & Guidetti R. 2009. DNA barcoding in Tardigrada: the first case study on Macrobiotus macrocalix Bertolani & Rebecchi 1993 (Eutardigrada, Macrobiotidae). Molecular Ecology Resources 9 (3): 699–706. https://doi.org/10.1111/j.1755-0998.2009.02538.x

Dastych H. 1980. Niesporczaki (Tardigrada) Tatrzańskiego Parku Narodowego. Monografie Fauny Polski 9, PWN, Krakow.

Dastych H. 1984. The Tardigrada from Antartica with description of several new species. Acta Zoologica Cracoviensia 27: 377–436.

Degma P. & Guidetti R. 2007. Notes to the current checklist of Tardigrada. Zootaxa 1579: 41–53.

Degma P., Bertolani R. & Guidetti R. 2009–2016. Actual checklist of Tardigrada species. (v. 31: 15 Dec. 2016). Available from www.tardigrada.modena.unimo.it/miscellanea/Actual%20checklist%20of%20Tardigrada.pdf [accessed 6 Apr. 2017].

De Oliveira Dias C. 1999. Morphological abnormalities of Acartia lilljeborgi (Copepoda, Crustacea) in the Espirito Santo Bay (E.S. Brazil). Hydrobiologia 394: 249–251. https://doi.org/10.1023/A:1003502624336

Elmoor-Loureiro L.M. 2004. Morphological abnormalities in the cladoceran Ilyocryptus spinifer (Apipucos Reservoir, Pernambuco State, Brazil). Brazilian Journal of Biology 64 (1): 53–58. https://doi.org/10.1590/S1519-69842004000100007

Folmer O., Black M., Hoeh W., Lutz R. & Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.

Fransozo A., Teixeira G.M., Gomes R.R., Silva J.C. & Bolla Jr. E.A. 2012. Ocorrência de anormalidades morfológicas externas em caranguejos marinhos (Decapoda, Brachyura) no litoral norte do estado de São Paulo. Acta Scientiarum – Biological Sciences 34 (1): 101–104.

Geslin E., Debenay J., Duleba W. & Bonetti C. 2002. Morphological abnormalities of foraminiferal tests in Brazilian environments: comparison between polluted and non-polluted areas. Marine Micropaleontology 45 (2): 151–168. https://doi.org/10.1016/S0377-8398(01)00042-1

Głowska E. & Skoracki M. 2009. Anomalous chaetotaxy in the quill mites Torotrogla merulae Skoracki et al., 2000 (Acari, Prostigmata, Syringophilidae). Acta Parasitologica 54 (4): 364–367. https://doi.org/10.2478/s11686-009-0046-y

Guidetti R. & Bertolani R. 2005. Tardigrade taxonomy: an updated check list of the taxa and a list of characters for their identification. Zootaxa 845: 1–46.

Guidetti R., Altiero T., Marchioro T., Sarzi Amadè L., Avdonina A.M., Bertolani R. & Rebecchi L. 2012. Form and function of the feeding apparatus in Eutardigrada (Tardigrada). Zoomorphology 131 (2): 127–148. https://doi.org/10.1007/s00435-012-0149-0

Guidetti R., Peluffo J.R., Rocha A.M., Cesari M. & Moly de Peluffo M.C. 2013. The morphological and molecular analyses of a new South American urban tardigrade offer new insights on the biological meaning of the Macrobiotus hufelandi group of species (Tardigrada: Macrobiotidae). Journal of Natural History 47: 2409–2426. https://doi.org/10.1080/00222933.2013.800610

Guil N. & Giribet G. 2012. A comprehensive molecular phylogeny of tardigrades - adding genes and taxa to a poorly resolved phylum-level phylogeny. Cladistics 28 (1): 21–49. https://doi.org/10.1111/j.1096-0031.2011.00364.x

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

Hebert P.D.N., Cywinska A., Ball S.L. & de Waard J.R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B 270: 313–322. https://doi.org/10.1098/rspb.2002.2218

Horning D.S., Schuster R.O. & Grigarick A.A. 1978. Tardigrada of New Zealand. New Zealand Journal of Zoology 5: 185–280. https://doi.org/10.1080/03014223.1978.10428316

Kaczmarek Ł., Goldyn B., Prokop Z.M. & Michalczyk Ł. 2011. New records of Tardigrada from Bulgaria with the description of Macrobiotus binieki sp. nov. (Eutardigrada: Macrobiotidae) and a key to the species of the harmsworthi group. Zootaxa 2781: 29–39.

Kaczmarek Ł., Jakubowska N. & Michalczyk Ł. 2012. Current knowledge on Turkish tardigrades with a description of Milnesium beasleyi sp. nov. (Eutardigrada: Apochela: Milnesiidae, the granulatum group). Zootaxa 3589: 49–64.

Kaczmarek Ł., Cytan J., Zawierucha K., Diduszko D. & Michalczyk Ł. 2014. Tardigrades from Peru (South America), with descriptions of three new species of Parachela. Zootaxa 3790 (2): 357–379. https://doi.org/10.11646/zootaxa.3790.2.5

Kaczmarek Ł., Michalczyk Ł. & McInnes S.J. 2015. Annotated zoogeography of non-marine Tardigrada. Part II: South America. Zootaxa 3923 (1): 1–107. https://doi.org/10.11646/zootaxa.3923.1.1

Kaczmarek Ł., Michalczyk Ł. & McInnes S.J. 2016. Annotated zoogeography of non-marine Tardigrada. Part III: North America and Greenland. Zootaxa 4203 (1): 001–249. https://doi.org/10.11646/zootaxa.4203.1.1

Londoño R., Daza A., Caicedo M., Quiroga S. & Kaczmarek Ł. 2015. The genus Milnesium (Eutardigrada: Milnesiidae) in the Sierra Nevada de Santa Marta (Colombia), with the description of Milnesium kogui sp. nov. Zootaxa 3955 (4): 561–568. https://doi.org/10.11646/zootaxa.3955.4.7

Marley N.J., McInnes S.J. & Sands C.J. 2011. Phylum Tardigrada: a re-evaluation of the Parachela. Zootaxa 2819: 51–64.

McInnes S.J. 1994. Zoogeographic distribution of terrestrial/freshwater tardigrades from current literature. Journal of Natural History 28: 257–352. https://doi.org/10.1080/00222939400770131

Méndez-de Daboín Y., Oviedo-Araújo M., González-Pérez A., Suárez-Hernández J., Sandoval C.M. & Cazorla D. 2015. Anomalías morfológicas en los dientes del cibario de Lutzomyia evansi (Diptera: Psychodidae) en el estado Trujillo, Venezuela. Biomedica 35 (2): 269–273.

Meriç E., Avşar N., Yokeş M.B., Tuǧrul A.B., Bayari S., Özyurt N., Barut I.F., Balkis N., Uysal K. & Kam E. 2008. Morphological abnormalities in benthic foraminifers of the Antalya coast. Micro-paleontology 54 (3–4): 241–276.

Michalczyk Ł. & Kaczmarek Ł. 2003. A description of the new tardigrade Macrobiotus reinhardti (Eutardigrada: Macrobiotidae, harmsworthi group) with some remarks on the oral cavity armature within the genus Macrobiotus Schultze. Zootaxa 331: 1–24.

Michalczyk Ł. & Kaczmarek Ł. 2013. The Tardigrada Register: a comprehensive online data repository for tardigrade taxonomy. Journal of Limnology 72 (S1): 175–181. https://doi.org/10.4081/jlimnol.2013.s1.e22

Michalczyk Ł., Wełnicz W., Frohme M. & Kaczmarek Ł. 2012. Redescriptions of three Milnesium Doyère, 1840 taxa (Tardigrada: Eutardigrada: Milnesiidae), including the nominal species for the genus. Zootaxa 3154: 1–20.

Miličić D., Pavković-Lučić S. & Lučić L. 2013. On some morphological abnormalities in adult fairy shrimp Branchipus schaefferi Fischer, 1834, from Serbia. Archives of Biological Sciences 65 (4): 1645–1650. https://doi.org/10.2298/ABS1304645M

Mironov S.V., Dabert J. & Dabert M. 2012. A new feather mite species of the genus Proctophyllodes Robin, 1877 (Astigmata: Proctophyllodidae) from the Long-tailed Tit Aegithalos caudatus (Passeri-formes: Aegithalidae): morphological description with DNA barcode data. Zootaxa 3253: 54–61.

Morek W., Gąsiorek P., Stec D., Blagden B & Michalczyk Ł. 2016. Experimental taxonomy exposes ontogenetic variability and elucidates the taxonomic value of claw configuration in Milnesium Doyère, 1840 (Tardigrada: Eutardigrada: Apochela). Contributions to Zoology 85 (2): 173–200.

Nelson D.R., Guidetti R. & Rebecchi L. 2015. Chapter 17: Phylum Tardigrada. In: Thorp J. & Rogers D.C. (eds) Ecology and General Biology. Vol. 1: 347–380. Thorp and Covich’s Freshwater Invertebrates (4th edition), Elsevier, Amsterdam.

Pilato G. 1981. Analisi di nuovi caratteri nello studio degli Eutardigradi. Animalia 8: 51–57.

Pilato G. & Binda M.G. 1996. Two new species and new records of Macrobiotus (Eutardigrada) from New Zealand. New Zealand Journal of Zoology 23: 375–379.

Pilato G. & Binda M.G. 2010. Definition of families, subfamilies, genera and subgenera of the Eutardigrada, and keys to their identification. Zootaxa 2404: 1–52.

Ramazzotti G. & Maucci W. 1983. Il Phylum Tardigrada. Memorie dell’Istituto Italiano di Idrobiologia, Pallanza 41, Istituto Italiano di Idrobiologia, Verbania.

Reinert J.F. 1999. Morphological abnormalities in species of the quadrimaculatus complex of Anopheles (Diptera: Culicidae). Journal of the American Mosquito Control Association 15 (1): 8–14.

Roszkowska M., Ostrowska M. & Kaczmarek Ł. 2015. The genus Milnesium Doyère, 1840 (Tardigrada) in South America with descriptions of two new species from Argentina and discussion of the feeding behaviour in the family Milnesiidae. Zoological Studies 54: 1–17. https://doi.org/10.1186/s40555-014-0082-7

Roszkowska M., Stec D., Ciobanu D.A. & Kaczmarek Ł. 2016. Tardigrades from Nahuel Huapi National Park (Argentina, South America) with descriptions of two new Macrobiotidae species. Zootaxa 4105 (3): 243–260. https://doi.org/10.11646/zootaxa.4105.3.2

Samir A.M. & El-Din A.B. 2001. Benthic foraminiferal assemblages and morphological abnormalities as pollution proxies in two Egyptian bays. Marine Micropaleontology 41 (3-4): 193–227. https://doi.org/10.1016/S0377-8398(00)00061-X

Sands C.J., Mcinnes S.J., Marley N.J., Goodall-Copestake W., Convey P. & Linse K. 2008. Phylum Tardigarda: an “individual” approach. Cladistics 24 (6): 861–871. https://doi.org/10.1111/j.1096-0031.2008.00219.x

Schill R.O., Forster F., Dandekar T. & Wolf N. 2010. Using compensatory base change analysis of internal transcribed spacer 2 secondary structures to identify three new species in Paramacrobiotus (Tardigrada). Organisms Diversity & Evolution 10 (4): 287–296. https://doi.org/10.1007/s13127-010-0025-z

Stec D., Smolak R., Kaczmarek Ł. & Michalczyk Ł. 2015. An integrative description of Macrobiotus paulinae sp. nov. (Tardigrada: Eutardigrada: Macrobiotidae: hufelandi group) from Kenya. Zootaxa 4052 (5): 501–526. https://doi.org/10.11646/zootaxa.4052.5.1

Stec D., Gąsiorek P., Morek W., Kosztyła P., Zawierucha K., Michno K., Kaczmarek Ł., Prokop Z.M. & Michalczyk Ł. 2016a. Estimating optimal sample size for tardigrade morphometry. Zoological Journal of the Linnean Society 178 (4): 776–784. https://doi.org/10.1111/zoj.12404

Stec D., Morek W., Gąsiorek P., Kaczmarek Ł. & Michalczyk Ł. 2016b. Determinants and taxo-nomic consequences of extreme egg shell variability in Ramazzottius subanomalus (Biserov, 1985) (Tardigrada). Zootaxa 4208 (2): 176–188. https://doi.org/10.11646/zootaxa.4208.2.5

St Louis R., Burningham L., Dowl A. & Grosberg M. 2009. Lonely Planet Guide: Ecuador & the Galápagos Islands. Lonely Planet, New York.

Tamura K., Dudley J., Nei M. & Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599. https://doi.org/10.1093/molbev/msm092

Thompson J.D., Higgins D.G. & Gibson T.J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positionspecific gap penalties and weight matrix choice. Nucleic Acids Research 22 (22): 4673–80.

Tumanov D.V. 2006. Five new species of the genus Milnesium (Tardigrada, Eutardigrada, Milnesiidae). Zootaxa 1122: 1–23.

Vicente F. & Bertolani R. 2013. Considerations on the taxonomy of the Phylum Tardigrada. Zootaxa 3626: 245–248. https://doi.org/10.11646/zootaxa.3626.2.2

Wełnicz W., Grohme M.A., Kaczmarek Ł., Schill R.O. & Frohme M. 2011. ITS-2 and 18S rRNA data from Macrobiotus polonicus and Milnesium tardigradum (Eutardigrada, Tardigrada). Journal of Zoological Systematics and Evolutionary Research 49 (S1): 34–39. https://doi.org/10.1111/j.1439-0469.2010.00595.x

White T.J., Bruns T., Lee S. & Taylor J. 1990. PCR protocols: a guide to methods and application: 315–322. Academic Press, San Diego, California.

Zagal C.J. 2008. Morphological abnormalities in the stauromedusa Haliclystus auricula (Cnidaria) and their possible causes. Journal of the Marine Biological Association of the United Kingdom 88 (2): 259–262. https://doi.org/10.1017/S0025315408000179


Refbacks

  • There are currently no refbacks.


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