Two deep-living rhodaliids (Cnidaria, Siphonophora) from the Mid-Atlantic Ridge

<p>Rhodaliids are a semi-benthic family of 14 physonect siphonophore species found in all oceans, except the Mediterranean and Arctic. They inhabit species-specific depth ranges in isolated locations and records are mostly sparse. Here, the first ever observations of rhodaliids from the Mid-Atlantic Ridge are given, from three images of two putative species. They come from depths of 3482 and 3667–3670 metres, on the Mid-Atlantic Ridge (MAR) at 23°N and 26°N, near two hydrothermal vents. Rhodaliids are very delicate animals and extremely hard to sample, particularly from such great depths, and the only comparable deep-living species so far described is the Galapagos Dandelion (<i>Thermopalia taraxaca</i>) from 2480–2938 metres on the Galapagos Rift and East Pacific Rise. This species inhabits the outer zone of certain hydrothermal vents where there is no hydrogen sulphide in the water, but connectivity with the MAR species is unlikely, since the latter inhabit a different ocean basin. Two, or possibly three, rhodaliid species have so far been collected in the North Atlantic, and all occurred near continental margins. These new observations are therefore important, and the images included here will hopefully alert future expeditions to hunt for, and perhaps even collect, more specimens. Rhodaliids are mostly observed individually adhering to a variety of substrata with their long tentacles, but very occasionally abundances of from 1 to 11 individuals m⁻² have been noted. Rhodaliids feed on copepods, other small pelagic crustaceans and fish larvae, and can thus represent important members of deep-sea ecosystems. This paper provides a distribution map of all species with an accompanying table showing coordinates, depths and number of specimens collected, and a second table of comparative diagnostic rhodaliid characters, which is used to suggest possible identities for the two putative new MAR species.</p

Temporal distribution of Cambrian arthropods conventionally assigned to the Bradoriida and Phosphatocopida.

<p>Bradoriid ranges are compiled from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Williams5" target="_blank">[57]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Zhang1" target="_blank">[71]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Topper1" target="_blank">[72]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Dieslvarez1" target="_blank">[78]</a> and references therein, representing a global dataset. Thick lines indicate definite ranges, whilst thin lines represent a questionable or imprecisely defined range. Only data from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Hou2" target="_blank">[46]</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Zhang1" target="_blank">[71]</a> are used to reconstruct the ranges of Bradoriida from China. The phosphatocopid data are from China <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Hou2" target="_blank">[46]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Zhang2" target="_blank">[77]</a>, Britain <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Williams3" target="_blank">[43]</a>, Scandinavia and north Germany <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Maas1" target="_blank">[13]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-HinzSchallreuter1" target="_blank">[56]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Ahlberg2" target="_blank">[63]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Terfelt1" target="_blank">[73]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-HinzSchallreuter2" target="_blank">[79]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Grndel1" target="_blank">[80]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-HinzSchallreuter3" target="_blank">[81]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-HinzSchallreuter4" target="_blank">[82]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-BergMadsen1" target="_blank">[83]</a>: phosphatocopids are also known from the Antarctic <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Wrona1" target="_blank">[74]</a>, North America <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Siveter9" target="_blank">[66]</a>, Australia <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Jago1" target="_blank">[84]</a> and Kazakhstan <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Melnikova1" target="_blank">[75]</a>. The Borregård Member of Bornholm (equivalent to the Exsulans Limestone) was originally identified as the oldest horizon in Scandinavia with the phosphatocopids <i>Hesslandona</i>, <i>Vestrogothia</i>, <i>Bidimorpha</i> and <i>Falites </i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-HinzSchallreuter2" target="_blank">[79]</a>. The Borregård Member is equivalent to the <i>P. gibbus</i> Biozone of uppermost Stage 5 <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Rushton1" target="_blank">[47]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-BergMadsen1" target="_blank">[83]</a>. However, later the same author <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-HinzSchallreuter4" target="_blank">[82, p. 887]</a> referred the material of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-HinzSchallreuter2" target="_blank">[79]</a> to the ‘Andrarum Limestone Breccia’, a horizon equivalent to the <i>P. forchhammeri</i> Biozone. Accordingly, we take the lower ranges of these phosphatocopids as Guzhangian. Our range for <i>Waldoria</i> includes material referred to <i>Falidoria</i> in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-HinzSchallreuter4" target="_blank">[82]</a>. We plot genera as a proxy for species diversity. This is reasonable given that most bradoriid genera contain only between 1 and 3 species. Exceptions to this include <i>Cambria</i>, <i>Liangshanella</i>, <i>Anabarochilina</i>, <i>Indiana</i> and <i>Hipponicharion</i>. For phosphatocopids, a multitude of species are referred to <i>Dabashanella</i>, but most of these are synonyms of <i>D. hemicyclica </i><a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Hou2" target="_blank">[46]</a>. Later Cambrian phosphatocopids including <i>Falites</i>, <i>Cyclotron</i>, <i>Hesslandona</i>, <i>Vestrogothia</i> and <i>Bidimorpha</i> all contain more than 3 species <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Dieslvarez1" target="_blank">[78]</a>, emphasising the diversity of Guzhangian and Pabian phosphatocopid assemblages. Also shown are the major Carbon Isotope Excursions (CIEs) after <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Zhu1" target="_blank">[58]</a>, and oxygen levels reconstructed from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Saltzman1" target="_blank">[3]</a>. For the latter, the red line represents the oxygen reconstruction (with error shown in pink envelope) of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Saltzman1" target="_blank">[3]</a> and the blue line [with error envelope] is the Berner reconstruction quoted therein. In the text and figures we use the terms ‘early’, ‘middle’ and ‘late’ Cambrian informally to denote Cambrian Series 1 and 2 combined, Series 3, and Series 4 respectively. Note that some authors <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Maas1" target="_blank">[13]</a> would tentatively include <i>Epactridion</i>, <i>Dielymella</i>, <i>Liangshanella</i>, <i>Flemingopsis</i>, <i>Alutella</i>, <i>Oepikaluta</i> and <i>Gladioscutum</i> in the Phosphatocopida. For morphological reasons outlined in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Williams5" target="_blank">[57]</a> we include these taxa within the Bradoriida. Abbreviations for CIEs are: BAsal Cambrian Carbon isotope Excursion (BACE); ZHUjiaqing Carbon isotope Excursion (ZHUCE); SHIyantou Carbon isotope Excursion (SHICE); Cambrian Arthropod Radiation isotope Excursion (CARE); MIngxinsi Carbon Isotope Excursion (MICE); Archaeocyathid Extinction Carbon isotope Excursion (AECE); Redlichiid-Olenellid Extinction Carbon isotope Excursion (ROECE); Drumian Carbon isotope Excursion (DICE); StePtoean Carbon Isotope Excursion (SPICE); Top of Cambrian Excursion (TOCE).</p

Early ostracods from the Cambrian and Ordovician.

<p>A, <i>Kimsella luciae</i> Salas, Vannier & Williams, lateral view of right valve. Tremadocian, lower part of the Parcha Formation, Abra de Sococha Section, Province of Salta, Argentina, CORD-MP 11186. B, <i>Altajanella costulata</i> Melnikova, lateral view of right valve. Late Cambrian, Tandoshka Formation, Gorny Altay, PIN N4346/1. C, <i>Vojbokalina magnifica</i> Melnikova, left lateral view of carapace. Middle Cambrian, Leningrad Region, Russia, PIN N4341/6. D, <i>Nanopsis coquina</i> Salas, Vannier & Williams, lateral view of left valve. Tremadocian, Upper Member of the Coquena Formation, Quebrada Chalala Section, Cordillera Oriental, Argentina, CORD-MP 11179. Scale bars are: 100 µm. For repositories of figured specimens see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Williams2" target="_blank">[20]</a>.</p

Chronostratigraphy for the Cambrian.

<p>Correlation of regional stratigraphies (modified from <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Zhu1" target="_blank">[58]</a>) provides the key to understanding the bradoriid and phosphatocopid ranges reconstructed for <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone-0028183-g004" target="_blank">Figure 4</a>.</p

Recent ostracods with gills.

<p><i>Leuroleberis surugaensis</i> Hiruta from Japan. A–C, scanning electron micrographs showing book gills in the branchial cavities, left lateral and posterior views. D, gill in transmitted light showing internal hemolymph sinuses. E, F, stained microtome serial sections, showing 8 pairs of gills on both sides of the soft body and detailed features through individual gills (e.g. hemolymph sinuses). Scale bars: 1 mm in A and B, 500 µm in D and E, 200 µm in C, and 50 µm in F. bg, book gill (integumental lamina attached to thoracic wall); ef, epipodial fan for ventilation; hs, hemolymph sinus in book gills.</p

General morphology of bradoriid arthropods.

<p>A, B, <i>Kunmingella douvillei</i> (Mansuy) from the early Cambrian Maotianshan Shale, Yunnan Province, China, dorsal views of two specimens showing bivalved open carapace in “butterfly” position and posterior appendages, Chen Jun-Yuan's personal collections, Chengjiang and RCCBYU 10258, respectively (B, courtesy of Derek Siveter). C, <i>Anabarochilina</i> sp., middle Cambrian from Kazakhstan, PIN N4343/55, partly exfoliated right valve. D, <i>Anabarochilina primordialis</i> (Linnarsson), middle Cambrian from Västergötland, Sweden, SGU 8662, partly exfoliated right valve. E, <i>Tsunyiella gridinae</i> Melnikova from the early Cambrian (Atdabanian) of North Central Kazakhstan, PIN N4343/12, left valve, internal mould. F, <i>Cambria melnikovi</i> Ivanova from the early Cambrian (Atdabanian) of the eastern part of Siberia, Russia, PIN N2175/1, largely exfoliated left valve. Small white arrows indicate supposed integumental hemolymph networks (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Vannier5" target="_blank">[51]</a>). All scale bars: 1 mm. For repositories of figured specimens see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Hou1" target="_blank">[14]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Melnikova1" target="_blank">[75]</a>.</p

Respiration in water-breathers from simple gaseous diffusion (1) to ventilatory and circulatory convection (5).

<p>PwO₂, PeO₂, PcellO₂, Pw′O₂, PaO₂, PvO₂ correspond to the partial pressure of oxygen in water, in the extracellular medium, at cell level, within external chamber (e.g. branchial chamber), in arterial hemolymph, and in venous hemolymph. Today, the PO₂ in the blood and tissues of water-breathing animals (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Massabuau1" target="_blank">[4]</a> for a review), is remarkably low, ranging between 1 and 3 kPa and is largely independent of ambient PO₂. PcellO₂ results from the equilibrium between O₂ supply and O₂ consumption (90% by mitochondria). PwO₂>Pw′O₂>PaO₂>PeO₂>PcellO₂.</p

General morphology of Recent ostracods exemplified by myodocopids.

<p>A, B, <i>Vargula hilgendorfii</i> (Müller), left lateral view of live female carrying embryos in her domiciliar cavity (carapace translucent) and lateral view of left valve in transmitted light showing the gas-exchange area, an integumental hemolymph network (yellow arrows indicate hemolymph circulation). C, <i>Azygocypridina</i> sp. from New Caledonia, France. Scanning electron micrograph showing appendages, left valve removed, including the ventilatory plates (courtesy of Vincent Perrier). D, E, transverse section through the carapace of <i>Vargula hilgendorfii</i> showing hemolymph sinuses, stained microtome serial section and scanning electron micrograph, respectively (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Vannier5" target="_blank">[51]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Abe1" target="_blank">[76]</a>). Scale bars: 1 mm in A–C, and 20 µm in D and E. ef, epipodial fan for ventilation; hs, hemolymph sinus; il, inner lamella; ol, outer lamella.</p

General morphology of phosphatocopid arthropods.

<p>A, <i>Hesslandona angustata</i> from the late Cambrian of western Hunan, China, ventral view of complete specimen with phosphatised appendages (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Zhang2" target="_blank">[77]</a>). B, <i>Klausmuelleria salopiensis</i> Siveter, Waloszek & Williams from the Protolenus-Strenuella Limestone, early Cambrian (Series 2), Shropshire England, reconstruction of appendages in ventral view (courtesy of Dieter Waloszek, Ulm). Reconstruction is based on a specimen 0.34 mm long <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0028183#pone.0028183-Siveter1" target="_blank">[11]</a>. C, <i>Vestrogothia spinata</i> Müller, from the late Cambrian “Orsten” of Sweden, three-dimensional model, lateral and frontal views (courtesy of Joachim Haug). Scale bar: 100 µm.</p

Semi-thin sections of the digestive tract of <i>Idas iwaotakii</i>.

<p>The specimen was collected on turtle bone off New Caledonia. (A) Overall view of the digestive tract (longitudinal sections). The black arrow indicates the location of microvilli in the intestine. (B) Cross section of the oesophagus lined by a stratified epithelium. (C) Cross section of the intestine. (D) Cross section of the stomach lined by a cuboidal epithelium. The white arrow indicates the gastric shield. (E) Longitudinal section of a detail of intestinal contents.</p