Abstract
Specimens of Batillipes tubernatis Pollock, 1971 collected from the Portuguese coast (Lusitanian sea province) indicated a considerable southward extension in the distribution of the species along the northeast Atlantic Ocean. Based on the examination of these specimens and those of Pollock’s collection from the type locality (Scotland), it can also be concluded that the redescription of B. tubernatis based on specimens from the Gulf of Mexico (tropical northwest Atlantic Ocean) does not correspond to that species. Several differences, namely in the shape of cephalic appendages, toe discs and pattern of cuticular sculpture, clearly distinguish specimens of B. tubernatis from those collected in the Gulf of Mexico that certainly belong to a new unnamed species. Moreover, the examination of specimens previously collected in the southwest Atlantic Ocean (Brazil) and attributed to B. tubernatis showed that they belong to other undescribed new Batillipes species, suggesting that B. tubernatis does not occur in that region. Additionally, the only record from the temperate northwest Atlantic Ocean attributed to this species cannot be assigned to B. tubernatis either. Therefore, a clarification about the current taxonomic status of B. tubernatis is provided and a short characterisation of the habitat of this species on the Portuguese coast is presented. As the occurrence of the species outside the northeast Atlantic Ocean is questioned, this work should renew the discussion about trans- and cis-Atlantic distributions of meiobenthic species.
Similar content being viewed by others
References
Accogli G, Gallo M, D’Addabbo R, Hansen JG (2011) Diversity and ecology of the marine tardigrades along the Apulian coast. J Zool Syst Evol Res 49(Suppl 1):53–57
Anderson MJ (2001) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639
Anderson MJ (2002) DISTLM v.2: a FORTRAN computer program to calculate a distance-based multivariate analysis for a linear model. Department of Statistics, University of Auckland
Boeckner MJ, Sharma J, Proctor HC (2009) Revisiting the meiofauna paradox: dispersal and colonization of nematodes and other meiofaunal organisms in low- and high-energy environments. Hydrobiologia 624:91–106
Buchanan JB (1984) Sediment analysis. In: Holme NA, McIntyre AD (eds) Methods for the study of marine benthos. Blackwell, Oxford, pp 41–65
D’Addabbo Gallo M, Morone De Lucia MR, Grimaldi de Zio S (1987) Heterotardigrada of the Amendolara shoal, high Ionian Sea. In: Bertolani R (ed) Biology of tardigrades. Selected symposia and monographs U.Z.I., vol 1. Mucchi, Modena, pp 103–110
da Rocha CMC, Verçosa MM, dos Santos ECL, Barbosa DF, de Oliveira DAS, de Souza JRB (2009) Marine tardigrades from the coast of Pernambuco, Brazil. Meiofauna Mar 17:97–101
de Zio S (1962) Descrizione di Batillipes annulatus n. sp. e note su Batillipes pennaki Marcus, nuovo rinvenimento nel Mediterraneo (Heterotardigrada). Annuario dell’Istituto e Museo di Zoologia dell’Università di Napoli 14(6):1–7
Gallo D’Addabbo M, D’Addabbo R, Grimaldi de Zio S (2000) Redescription of Batillipes dicrocercus Pollock, 1970 and revision of the genus Batillipes (Tardigrada, Heterotardigrada). Zool Anz 239:329–339
Giere O (1993) Meiobenthology. The microscopic fauna in aquatic sediments. Springer-Verlag, Berlin
Grimaldi de Zio S, D’Addabbo Gallo M (1975) Reproductive cycle of Batillipes pennaki Marcus (Heterotardigrada) and observations on the morphology of the female genital apparatus. Pubbl Stazi Zool Napoli 39(Suppl):212–225
Grimaldi de Zio S, Morone De Lucia RM, D’Addabbo Gallo M (1984) Relazione tra morfologia ed ecologia nei tardigradi marini (Heterotardigrada–Arthrotardigrada). Cah Biol Mar 25:67–73
Grimaldi de Zio S, D’Addabbo Gallo M, Morone De Lucia MR (1987) Adaptive radiation and phylogenesis in marine Tardigrada and the establishment of Neostygarctidae, a new family of Heterotardigrada. Boll Zool 54:27–33
Höfling-Epiphanio E (1972) Ocorrência de Batillipes mirus Richters, 1909 e B. tubernatis Pollock, 1971 (tardigrada) no litoral brasileiro. Ciência e Cultura 24:358–359 (in Portuguese)
Hummon WD (1994) Trans- and cis-Atlantic distribution of three marine heterotardigrades. Trans Am Microsc Soc 113(3):333–342
Jørgensen A, Faurby S, Hansen JG, Møbjerg N, Kristensen RM (2010) Molecular phylogeny of Arthrotardigrada (Tardigrada). Mol Phylogenet Evol 54:1006–1015
Kaczmarek Ł, Bartels PJ, Roszkowska M, Nelson DR (2015) The zoogeography of marine Tardigrada. Zootaxa 4037(1):1–189
Kristensen RM (1978) Notes on marine Heterotardigrades I. Description of two new Batillipes species, using the electron microscope. Zool Anz 200:1–17
Kristensen RM, Mackness BS (2000) First record of the marine tardigrade genus Batillipes (Arthrotardigrada: Batillipedidae) from South Australia with a description of a new species. Rec South Aust Mus 33:73–87
Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24
Marcus E (1946) Batillipes pennaki, a new marine tardigrade from the north and south American Atlantic coast. Com Zool Mus Hist Nat Montevideo 2:1–3
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297
McGinty MM, Higgins RP (1968) Ontogenetic variation of taxonomic characters of two marine tardigrades with the description of Batillipes bullacaudatus n. sp. Trans Am Microsc Soc 87:252–262
McIntyre AD, Eleftheriou A (1968) The bottom fauna of a flatfish nursery ground. J Mar Biol Assoc UK 48:113–142
McIntyre AD, Murison DJ (1973) The meiofauna of a flatfish nursery ground. J Mar Biol Assoc UK 53(1):93–118
McKirdy DJ (1975) Batillipes (Heterotardigrada): comparison of six species from Florida (USA) and a discussion of taxonomic characters within the genus. In: International symposium on Tardigrades, 1974. Mem Ist Ital Idrobiol 32(Suppl):177–223
Menechella AG, Bulnes VN, Cazzaniga NJ (2015) A new Batillipedidae (Tardigrada, Arthrotardigrada) from Argentina. Zootaxa 4032(3):339–344
Moore CG (1979) The distribution and ecology of psammollittoral meiofauna around the Isle of Man. Cah Biol Mar 20:383–415
Morgan CI (1980) Notes on the distribution and abundance of the Irish marine Tardigrada, including two additions to the Irish fauna. Irish Nat J 20:148–152
Morgan CI, Lampard DJ (1986a) The fauna of the Clyde Sea area: phylum Tardigrada. University Marine Biological Station, Millport, 40 pp
Morgan CI, Lampard DJ (1986b) A wealth of water bears. Arran Nat 9:24–30
Morone De Lucia RM, D’Addabbo Gallo M, Grimaldi de Zio S (1988) Descrizione di due nuove specie di Batillipedidae (Tardigrada: Heterotardigrada). Cah Biol Mar 29:361–373
Pfannkuche O, Thiel H (1988) Sample processing. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 134–145
Pollock LW (1970) Batillipes dicrocercus n. sp., Stygarctus granulatus n. sp. and other Tardigrada from Woods Hole, Massachusetts, USA. Trans Am Microsc Soc 89(1):38–52
Pollock LW (1971) On some British marine Tardigrada, including two new species of Batillipes. J Mar Biol Assoc UK 51:93–103. https://doi.org/10.1017/s0025315400006482
Ramazzotti G (1962) Il Phylum Tardigrada. Mem Ist Ital Idrobiol 14:1–595
Renaud-Mornant J (1980) Description de trois espèces nouvelles du genre Tanarctus Renaud-Debyser, 1959, et création de la sous-famille des Tanarctinae, subfam. nov. (Tardigrada, Heterotardigrada). Bull Mus Natl Hist Nat 2(1):129–142
Renaud-Mornant J, Pollock LW (1971) A review of the systematics and ecology of marine Tardigrada. In: Hulings NC (ed) Proceedings of the First International Conference on Meiofauna. Smithsonian Contrib Zool 76:109–117
Richters F (1909) Marine Tardigraden. Verh Dtsch Zool Ges 19:84–95
Riemann F (1966) Die interstitielle Fauna im Elbe-Aestuar. Verbreitung und Systematik. Arch Hydrobiol Suppl 31:1–279
Rubal M, Veiga P, Fontoura P, Santos E, Sousa-Pinto I (2016) Biodiversity of marine tardigrades from the northern coast of Portugal (Iberian peninsula). Zool J Linn Soc Lond 178(4):747–754
Rubal M, Veiga P, Fontoura P, Sousa-Pinto I (2017) A new Batillipes (Tardigrada, Heterotardigrada, Batillipedidae) from North Portugal (Atlantic Ocean). Mar Biodivers 47:921–928. https://doi.org/10.1007/s12526-016-0526-x
Santana-e-Silva LG, Gomes Júnior EL, da Silva Gomes EP, da Rocha CMC (2010) Tardigrada de ecossistema recifal na Praia de Cupe (Ipojuca, PE). X Jornada de Ensino, Pesquisa e Extensão (JEPEX, 2010), UFRPE, Recife, 18 a 22 de Outubro (in Portuguese)
Santos E, da Rocha CMC, Gomes-Junior E, Fontoura P (2017) Three new Batillipes species (Arthrotardigrada: Batillipedidae) from the Brazilian coast. Zootaxa 4243(3):483–502. https://doi.org/10.11646/zootaxa.4243.3.4
Schmidt H, Westheide W (1999) Genetic relationships (RAPD-PCR) between geographically separated populations of the “cosmopolitan” interstitial polychaete Hesionides gohari (Hesionidae) and the evolutionary origin of the freshwater species Hesionides riegerorum. Biol Bull 196:216–226
Schmidt H, Westheide W (2000) Are the meiofaunal polychaetes Hesionides arenaria and Stygocapitella subterranea true cosmopolitan species?—Results of RAPD-PCR investigations. Zool Scripta 29(1):17–27
Schulz E (1955) Studien an marinen tardigraden. Kiel Meeresf 11:74–79
Sterrer W (1973) Plate tectonics as a mechanism for dispersal and speciation in interstitial sand fauna. Neth J Sea Res 7:200–222
Villora-Moreno S, Grimaldi de Zio S (1993) Redescription and ecology of Batillipes phreaticus Renaud-Debyser, 1959 (Arthrotardigrada, Batillipedidae) in the gulf of Valencia (western Mediterranean). Cah Biol Mar 34:387–399
Zawierucha K, Grzelak K, Kotwicki L, Kaczmarek Ł, Kristensen RM (2015) First observation of the marine tardigrades Batillipes mirus and Batillipes noerrevangi (Arthrotardigrada, Batillipedidae) from a strongly brackish part of the Polish Baltic Sea coast. Mar Biol Res 11(8):859–868. https://doi.org/10.1080/17451000.2015.1024133
Acknowledgements
The authors are grateful to Leland W. Pollock for donating his entire marine tardigrade collection, including B. tubernatis.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This research was partially funded by Polis Litoral Norte, S.A. through the project “Estudo de caracterização da actividade pesqueira costeira e dos seus impactes nos recursos e nas comunidades marinhas do Litoral Norte”, the European Regional Development Fund (ERDF) through the programme POFC-COMPETE, Quadro de Referência Estratégico Nacional (QREN) and also by the Fundação para a Ciência e Tecnologia (FCT), Portugal, through the project Pest-C/MAR/LA0015/2011 and through the strategic project UID/MAR/04292/2013 granted to the Marine and Environmental Sciences Centre (MARE). During this study, M. Rubal (SFRH/BDP/104225/2014) and P. Veiga (SFRH/BPD/81582/2011) were supported by postdoctoral grants awarded by Fundação para a Ciência e Tecnologia and É. Santos (BEX 13580/13-2) by a doctoral grant awarded by the programme Science Without Borders from the Coordination for the Improvement of Higher Education Personnel, Brazil (CAPES).
Conflict of Interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international and national guidelines for the care and use of animals were followed by the authors.
Additional information
Communicated by P. Martinez Arbizu
Rights and permissions
About this article
Cite this article
Santos, É., Rubal, M., Veiga, P. et al. On the distribution of Batillipes tubernatis Pollock, 1971 (Arthrotardigrada: Batillipedidae) in the Atlantic Basin. Mar Biodiv 49, 621–631 (2019). https://doi.org/10.1007/s12526-017-0834-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12526-017-0834-9