Review Article |
Corresponding author: Erica DeMilio ( erica.demilio@gmail.com ) Academic editor: Sandra McInnes
© 2016 Erica DeMilio, Colin Lawton, Nigel J. Marley.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
DeMilio E, Lawton C, Marley NJ (2016) Tardigrada of Ireland: a review of records and an updated checklist of species including a new addition to the Irish fauna. ZooKeys 616: 77-101. https://doi.org/10.3897/zookeys.616.8222
|
The phylum Tardigrada was not recorded in Ireland until the Clare Island Survey of 1909–1911, with only rare subsequent reports on Irish tardigrade species. In recent decades, significant taxonomic revision has occurred within Tardigrada. This has resulted in the need for a review of all known historical records from Ireland and Northern Ireland in order to produce an updated checklist of valid taxa. The new checklist includes fifty-one tardigrade species and subspecies including a new addition to the Irish fauna reported herein, Echiniscus quadrispinosus quadrispinosus Richters, 1902 from Newtown, Ballyvaughan, Co. Clare.
Tardigrada , Ireland, species list, historical records
Tardigrades, commonly known as “water bears”, are microscopic metazoans with body lengths typically between 0.1–1.2 mm. They are obligate aquatic organisms, occurring in marine, freshwater and damp terrestrial habitats such as soils, mosses and lichens. The body is cylindrical with four pairs of lobopodous appendages ending in claws or “toed” digits in many marine forms. Tardigrades are best known for the remarkable survival capabilities of many species through cryptobiosis, a type of quiescence that is also seen among other groups of microscopic animals found in similar habitats, notably Rotifera and Nematoda (for further information on tardigrade cryptobiosis see e.g.
Phylum Tardigrada has had a history of rearrangement, both in terms of its relative taxonomic position as well as its internal structure. Traditionally, Tardigrada was ranked as a class of Arthropoda until being recognised as a separate phylum by
The main intra-phylum division occurs between the classes Heterotardigrada Marcus, 1927 and Eutardigrada Richters, 1926. The heterotardigrades are a group of species that possess a particular cephalic structure known as cirrus A, they also have a separate gonopore and anus, and often have plated cuticles. Eutardigrade species lack cirrus A, have a cloaca, and cuticles without structures homologous to the sclerified plates present among heterotardigrades. A third monospecific class, Mesotardigrada, was described by
The Heterotardigrada are divided into two orders, the marine Arthrotardigrada Marcus, 1927 and Echiniscoidea Richters, 1926. Echiniscoidea comprises four families: Echiniscoididae Kristensen & Hallas, 1980; Carphaniidae Binda & Kristensen, 1986; Oreellidae Puglia, 1959; and the speciose Echiniscidae Thulin, 1928. Of these, only Echiniscoididae is generally regarded as marine. Species of the other three families occur in limnic or limno-terrestrial environments.
There has been significant taxonomic rearrangement of the Eutardigrada including the establishment of many new genera and families, as well as many new species additions.
Within Parachela, the use of morphological analyses and molecular data by
The purpose of the following review is to address the taxonomic changes that have occurred for each Irish species since the time of their original recording. This review facilitated the creation of a valid checklist of Tardigrada species for Ireland and Northern Ireland.
There has been very little investigation into the status of Tardigrada in Ireland. Studies that included Irish tardigrades are limited to:
We updated the checklist of Irish species, which is presented in Table
A–B An updated checklist of Irish tardigrade species with primary and subsequent records for: AHeterotardigradaBEutardigrada. * Indicates type specimen.
1A Class Heterotardigrada Marcus, 1927
Species | Original Irish Record | Additional Irish records |
---|---|---|
Order Arthrotardigrada Marcus, 1927 | ||
Family Batillipedidae Ramazzotti, 1962 | ||
Batillipes mirus Richters, 1909b |
|
0 |
Batillipes phreaticus Renaud-Debyser, 1959 |
|
0 |
Batillipes tubernatis Pollock, 1971 |
|
0 |
Order Echiniscoidea Richters, 1926 | ||
Family Echiniscoididae Kristensen and Hallas, 1980 | ||
Echiniscoides sp. |
|
0 |
Echiniscoides sigismundi cf. sigismundi |
|
|
Family Echiniscidae Thulin, 1928 | ||
Bryodelphax parvulus Thulin, 1928 |
|
0 |
Cornechiniscus cornutus (Richters, 1907) |
|
0 |
Echiniscus columinis* Murray, 1911 |
|
0 |
Echiniscus granulatus (Doyère, 1840) |
|
|
Echiniscus militaris* Murray, 1911 |
|
0 |
Echiniscus quadrispinosus quadrispinosus Richters, 1902 | Present study, Newtown, Ballyvaughan, Co. Clare | 0 |
Echiniscus testudo (Doyère, 1840) |
|
|
Echiniscus trisetosus Cuénot, 1932 |
|
0 |
Pseudechiniscus cf. suillus |
|
0 |
Hypechiniscus gladiator gladiator (Murray, 1905a) |
|
0 |
Hypechiniscus exarmatus (Murray, 1907a) |
|
0 |
Total = 16 taxa |
Species | Original Irish Record | Additional Irish records |
---|---|---|
Order Apochela Schuster, Nelson, Grigarick, and Christenberry, 1980 | ||
Family Milnesiidae Ramazzotti, 1962 | ||
Milnesium sp. |
|
0 |
Milnesium cf. tardigradumtardigradum |
|
|
Order Parachela Schuster, Nelson, Grigarick, and Christenberry, 1980 | ||
Superfamily Hypsibioidea Pilato, 1969 in Sands, McInnes, Marley, Goodall-Copestake, Convey, and Linse, 2008 (amended by |
||
Family Calohypsibiidae Pilato, 1969 | ||
Calohypsibius ornatus (Richters, 1900) |
|
0 |
Calohypsibius verrucosus (Richters, 1900) |
|
0 |
Family Hypsibiidae Pilato, 1969 | ||
Subfamily Diphasconinae Dastych, 1992 | ||
Diphascon cf. chilenense |
|
0 |
Diphascon cf. pingue |
|
0 |
Subfamily Hypsibiinae Pilato, 1969 | ||
Hypsibius arcticus (Murray, 1907b) |
|
0 |
Hypsibius cf. dujardini |
|
|
Subfamily Itaquasconinae Bartoš in Rudescu, 1964 | ||
Adropion scoticum scoticum (Murray, 1905b) |
|
|
Mesocrista spitzbergensis (Richters, 1903) |
|
0 |
Platicrista angustata (Murray, 1905a) |
|
0 |
Subfamily Pilatobiinae Bertolani, Guidetti, Marchioro, Altiero, Rebecchi and Cesari, 2014 | ||
Pilatobius bullatus (Murray, 1905b) |
|
0 |
Pilatobius oculatus oculatus (Murray, 1906b) |
|
0 |
Family Microhypsibiidae Pilato, 1998 | ||
Fractonotus caelatus (Marcus, 1928) |
|
0 |
Microhypsibius truncatus Thulin, 1928 |
|
0 |
Family Ramazzottiidae Sands, McInnes, Marley, Goodall-Copestake, Convey, and Linse, 2008 | ||
Hebesuncus conjungens (Thulin, 1911) |
|
0 |
Superfamily Isohypsibioidea Sands, McInnes, Marley, Goodall-Copestake, Convey and Linse, 2008 (amended by |
||
Family Isohypsibiidae Sands, McInnes, Marley, Goodall-Copestake, Convey and Linse, 2008 | ||
Isohypsibius annulatus annulatus (Murray, 1905a) |
|
0 |
Isohypsibius panovi* Tumanov, 2005 |
|
0 |
Isohypsibius papillifer bulbosus (Marcus, 1928) |
|
0 |
Isohypsibius prosostomus prosostomus Thulin, 1928 |
|
|
Isohypsibius prosostomus cambrensis (Morgan, 1976) |
|
0 |
Isohypsibius schaudinni (Richters, 1909b) |
|
|
Isohypsibius tuberculatus (Plate, 1888) |
|
|
Thulinius augusti (Murray, 1907a) |
|
0 |
Superfamily Macrobiotoidea Thulin, 1928 in Sands, McInnes, Marley, Goodall-Copestake, Convey and Linse, 2008 | ||
Family Macrobiotidae Thulin, 1928 | ||
Macrobiotus crenulatus Richters, 1904c |
|
0 |
Macrobiotus echinogenitus Richters, 1903 |
|
0 |
Macrobiotus cf. harmsworthi |
|
|
Macrobiotus cf. hufelandi |
|
|
Macrobiotus occidentalis occidentalis Murray, 1910 |
|
0 |
Macrobiotus virgatus Murray, 1910 |
|
0 |
Minibiotus cf. intermedius |
|
|
Paramacrobiotus areolatus (Murray, 1907b) |
|
|
Paramacrobiotus richtersi* (Murray, 1911) |
|
|
Family Murrayidae Guidetti, Rebecchi and Bertolani, 2000 | ||
Murrayon hastatus (Murray, 1907a) |
|
0 |
Murrayon hibernicus* (Murray, 1911) |
|
0 |
Total = 35 taxa |
The study of Irish tardigrades began with the work of the Scottish biologist and explorer, James Murray, as part of the multidisciplinary survey of Clare Island located off the west coast of County Mayo, Ireland (
The nine other heterotardigrade species reported by
Other heterotardigrades that were recorded by
The last three heterotardigrade records by
Murray recorded twenty-five eutardigrade species in the Clare Island Survey (Table
The rest of Murray’s eutardigrade records are for Parachela. Following the convention of the time, Murray ascribed these species to only two long-standing genera, Diphascon Plate, 1888, differentiated by the presence of a flexible pharyngeal tube, or Macrobiotus C.A.S. Schultze, 1834. However, under the most current taxonomic scheme (
The specimens recorded by
Of the twenty-two other species attributed to Macrobiotus that were recorded by
Four of the “Macrobiotus” taxa
Another of
Two of
The remaining nine species from
Three of
The two other species, recorded from Clare Island itself, Macrobiotus areolatus Murray, 1907b and Macrobiotus richtersi Murray, 1911 (
The last two of
Following
New species records for Ireland did not occur until
The heterotardigrade order, Arthrotardigrada, was not recorded from Ireland until
Along with
Further details on species locations are given in two of Morgan’s subsequent works (
Further results from Morgan’s earlier Irish collections were published in 1976 (
More recently,
The most recent published data on Irish tardigrades are
A specimen, found in a sample of moss collected from a tree trunk along a rural road in Newtown, Ballyvaughan, Co. Clare (53°6.28'N; 9°10.18'W) in January 2013, was a new record for Ireland and is added to our checklist. The specimen was mounted with Polyvinyl Alcohol medium and identified using an Olympus BX53 microscope with magnification up to x1000 oil immersion. All measurements were taken using Olympus cellSens imaging software (Standard Version 1 CS-ST-V1).
A single adult individual was found (Figure
The authors wish to thank Louise Allcock, Wallace Arthur, Peter Degma, Jesper G. Hansen, Reinhardt M. Kristensen, Sandra J. McInnes, Nigel Monaghan, and Anne Marie Power for their assistance. We are especially grateful to our reviewers for the improvement of our manuscript with their valued comments. The James Hardiman Postgraduate Scholarship and the Irish Research Council provided funding for this work.