Iben Heiner

The first metazoa living in permanently anoxic conditions

BackgroundSeveral unicellular organisms (prokaryotes and protozoa) can live under permanently anoxic conditions. Although a few metazoans can survive temporarily in the absence of oxygen, it is believed that multi-cellular organisms cannot spend their entire life cycle without free oxygen. Deep seas include some of the most extreme ecosystems on Earth, such as the deep hypersaline anoxic basins of the Mediterranean Sea. These are permanently anoxic systems inhabited by a huge and partly unexplored microbial biodiversity.ResultsDuring the last ten years three oceanographic expeditions were conducted to search for the presence of living fauna in the sediments of the deep anoxic hypersaline LAtalante basin (Mediterranean Sea). We report here that the sediments of the LAtalante basin are inhabited by three species of the animal phylum Loricifera (Spinoloricus nov. sp., Rugiloricus nov. sp. and Pliciloricus nov. sp.) new to science. Using radioactive tracers, biochemical analyses, quantitative X-ray microanalysis and infrared spectroscopy, scanning and transmission electron microscopy observations on ultra-sections, we provide evidence that these organisms are metabolically active and show specific adaptations to the extreme conditions of the deep basin, such as the lack of mitochondria, and a large number of hydrogenosome-like organelles, associated with endosymbiotic prokaryotes.ConclusionsThis is the first evidence of a metazoan life cycle that is spent entirely in permanently anoxic sediments. Our findings allow us also to conclude that these metazoans live under anoxic conditions through an obligate anaerobic metabolism that is similar to that demonstrated so far only for unicellular eukaryotes. The discovery of these life forms opens new perspectives for the study of metazoan life in habitats lacking molecular oxygen.

Tubulideres seminoli gen. et sp. nov. and Zelinkaderes brightae sp. nov. (Kinorhyncha, Cyclorhagida) from Florida

One new kinorhynch genus and species and one new species from the genus Zelinkaderes are described from sandy sediment off Fort Pierce, Florida. The new genus and species, Tubulideres seminoli gen. et sp. nov. is characterized by the presence of the first trunk segment consisting of a closed ring, the second segment of a bent tergal plate with a midventral articulation and the following nine segments consisting of a tergal and two sternal plates. Cuspidate spines are not present, but flexible tubules are located on several segments, and in particular concentrated on the ventral side of the second segment. Middorsal spines are present on all trunk segments and are alternatingly offset to a position slightly lateral to the middorsal line. Zelinkaderes brightae nov. sp. is characterized by its spine formula in having middorsal spines on trunk segments 4, 6 and 8–11, lateroventral acicular spines on segment 2, lateral accessory cuspidate spines on segments 2 and 8, ventrolateral cuspidate spines on segments 4–6 and 9, lateroventral acicular spines present on segments 8 and 9, and midterminal, lateral terminal and lateral terminal accessory spines on segment 11. The spine formula of Z. brightae nov. sp. places it in a position in between Z. submersus and a clade consisting of Z. klepali and Z. floridensis. The new findings on Z. brightae nov. sp. have led us to propose an emended diagnosis for the genus.

Does fish from the Disko Bay area of Greenland possess antifreeze proteins during the summer

The blood of 21 teleosts and 1 elasmobranch was analysed for antifreeze-protein activity by determining the thermal hysteresis. The fish were caught in the summertime at different locations in West Greenland (Disko Bay area). The difference between the melting and hysteresis freezing point (thermal hysteresis) is a numerical indication of the presence of antifreeze-protein activity.No thermal hysteresis was detected in the blood of the elasmobranch, Raja radiata (thorny skate) and, as expected, its blood was isosmotic to seawater. Of the 21 teleost species examined, 11 were found to have a thermal hysteresis greater than 0.1°C, an indication of the presence of substantial amounts of antifreeze. The remaining 10 species had a hysteresis less than 0.1°C, and thus their summertime possession of antifreeze protein was concluded to be very low or absent. No hysteresis was detected in Gadus morhua (Atlantic cod), but there was a slight faceting of the seed crystal, indicative of a low, possibly physiologically unimportant, level of antifreeze protein.This study is the first time antifreeze-protein activity has been detected in the species Stichaeus punctatus (Arctic shanny).

A comparative morphological study of the kinorhynch genera Antygomonas and Semnoderes (Kinorhyncha: Cyclorhagida)

Detailed information revealed through combined use of light- and scanning electron microscopy, is given for two species of kinorhynchs, representing the cyclorhagid genera Semnoderes and Antygomonas. The two species have not previously been examined using SEM, and the new observations point out several similarities between species of the two genera, which could indicate a potential close relationship. The generated data is meant to be incorporated in a future phylogenetic analysis in order to clarify the phylogenetic relationships among kinorhynchs.

A new species of Echinoderes from Florida (Kinorhyncha: Cyclorhagida)

ABSTRACT A new kinorhynch, Echinoderes spinifurca, is described from the Atlantic coast off Fort Pierce, Florida. The species is characterized by the presence of middorsal spines on segments 6 to 10 and lateral spines/tubules on segments 4 and 7–12. The tergal furca (tergal extension) is extraordinarily long, constituting 9.3–12.9 percent of the trunk length, and this distinct character makes it easy to distinguish the species from all other species of Echinoderes. Echinoderes spinifurca occurs in shell gravel and mixed shell gravel with sand, and coexists with Echinoderes horni, Zelinkaderes sp., and two undescribed cyclorhagid taxa.

Urnaloricus gadi nov. gen. et nov. sp. (Loricifera, Urnaloricidae nov. fam.), an aberrant Loricifera with a viviparous pedogenetic life cycle

A new species of Loricifera, Urnaloricus gadi nov. gen. et nov. sp., is described from the Faroe Bank, located Southwest of the Faroe Islands, North Atlantic. The new species does not fit into any known families of Loricifera and therefore it is grouped into a new family Urnaloricidae nov. fam. The new species is characterized by having a very complicated life cycle that involves a large cyst‐like mega‐larva, two reduced larval instars and the Higgins‐larvae eating their maternal stage from within. An adult stage is missing. This form of reproduction is called viviparous pedogenesis and normally is found only in nematodes and insects. In the life cycle of Urnaloricidae nov. fam., there are two types of free‐living larval stages: a Higgins‐larva and a mega‐larva. The latter is found in two different forms, a pre‐ and a cyst‐forming mega‐larva. Additionally, there are two reduced life history stages, the reduced larval stage (probably a postlarva) and the ghost‐larval stage inside the cyst‐forming mega‐larva. The external morphology of the two forms of mega‐larvae is much reduced, e.g., the introvert has only a few rows of scalids when compared with the Higgins‐larva. The pre mega‐larva is free‐living and can sometimes be covered with coccoliths. Internally, a large ovary with a few oocytes, a digestive system, and an internal armature with retracted scalids are present. The pre mega‐larva presumably molts into a cyst‐forming mega‐larva and thereby the ovary is now seen inside the cyst‐forming mega‐larva. The cyst‐forming mega‐larva has the same structures as in the pre mega‐larva though here the scalids are protruded and there is a gonopore. Inside the cyst‐forming mega‐larva the ovary produces more oocytes and begins to fill out the entire lumen. At this stage the cyst‐forming mega‐larva molts first to the presumed postlarval stage, and then this stage molts to a ghost‐larva. Hence, the ovary now matures inside the ghost‐larva, which is surrounded by both the cuticle of the reduced postlarval stage and the cuticle of the cyst‐forming mega‐larva. The oocytes mature into eggs, and then into embryos and finally into Higgins‐larvae while reabsorbing all the tissue of their maternal stage, the ghost‐larva. During this maturation the cuticle of the cyst‐forming mega‐larva starts to harden and become cyst‐like. The fully developed Higgins‐larvae emerge through the gonopore of the cyst‐forming mega‐larva by penetrating the thin cuticles of the ghost‐larva and the postlarva. The embryos have holoblastic radial cleavage and later a fluid‐filled blastocoel is formed. The eggshells are extremely elastic; hence, they can become very elongated as the embryos mature into Higgins‐larvae. J. Morphol., 2009.

Loricifera from the deep sea at the Galápagos Spreading Center, with a description of Spinoloricus turbatio gen. et sp. nov. (Nanaloricidae)

Specimens of a new species of Loricifera, Spinoloricus turbatio gen. et sp. nov., have been collected at the Galápagos Spreading Center (GSC) during the cruise SO 158, which is a part of the MEGAPRINT project. The new genus is positioned in the family Nanaloricidae together with the three already described genera Nanaloricus, Armorloricus and Phoeniciloricus. The postlarvae and adults of Spinoloricus turbatio gen. et sp. nov. are characterized by a mouth cone with eight oral ridges and basally with a cuticular reinforcement named mouth cone pleat; eighth row with 30 whip-like spinoscalids and 30 “alternating” plates; thorax with eight single and seven double trichoscalids, where the single trichoscalids are twice the length of the double ones, and the secondary appendage on the double trichoscalid is smooth whereas the others are serrated; lorica with eight cuticular plates with additional spikes in the anterior corners and intercalary plicae between the plates. Some of these genus-specific characters such as the mouth cone pleat, the “alternating” plates and the intercalary plicae have not been observed in Nanaloricidae before. The Higgins-larvae of Spinoloricus turbatio gen. et sp. nov. are characterized by six rectangular plates in the seventh row with two teeth, an indistinct honeycomb sculpture and long toes with little mucrones. The SO 158 cruise has yielded a minimum of ten new species of Loricifera out of only 42 specimens. These new species belong to two different orders, where one being new to science, and three different families. This result indicates a high diversity of loriciferans at the GSC. Nearly all the collected loriciferans are in a moulting stage, hence there is a new stage inside the present stage. This prolongation of life stages and the occurrence of multiple life stages inside each other are typical of deep-sea loriciferans. Here exemplified by the two postlarvae with adults inside, which is observed for the first time in Nanaloricidae.

Armorloricus kristenseni (Nanaloricidae, Loricifera), a new species from the Faroe Bank (North Atlantic)

The year 2003 was the 20th anniversary of the description of the phylum Loricifera and of the type species Nanaloricus mysticus Kristensen, 1983, from Roscoff, France. To honour this occasion, a loriciferan of the newly described genus Armorloricus, from Roscoff, will be named after the discoverer of the phylum Loricifera, Professor Reinhardt Møbjerg Kristensen. This new species, Armorloricus kristenseni sp. nov., was found during two cruises to the Faroe Bank in the North Atlantic, in 1992 and 2001. The specimens were collected at three different stations (one in 1992 and two in 2001) all situated on the plateau itself at a depth of approximately 150xa0m. The adults are characterized by their elongated shape, the large lateral lorica plates, the very long, feather-like scalids in the third row, the long claspers in the male, and the wheel-like structure of the subcuticle glands inside the lorica plates on the ventral side. The Higgins-larvae are characterized by their long middorsal scalid with a hexagonal base and the small hook-shaped midventral pair of scalids in row 4. Furthermore, the long, paired, serrated scalids in row 6 and the asymmetrical basal plate with numerous teeth in row 7 are also unique characters. For an easier between-family comparison of the different scalids and rows on the introvert, the second row in the adults of Nanaloricidae has been split up into two rows, so that all adult loriciferans posses a total of nine rows on the introvert.

Rugiloricus bacatus sp. nov. (Loricifera ‐Pliciloricidae) and a ghost‐larva with paedogenetic reproduction

Abstract A new species of Loricifera, Rugiloricus bacatus sp. nov. is described together with the diagnoses of two other Rugiloricus species, Rugiloricus sp. nov. A and B, from the Faroe Bank (North Atlantic). Characteristic for all three species is the presence of a new type of reduced larva, a ghost‐larva. This type of reduced larva was discovered in 1986 by Jeanne Renaud‐Mornant, but it was with the Faroe Bank material that it was first discovered that the ghost‐larvae belonged to the phylum Loricifera. The ghost‐larvae are eitherfound inside late instar Higgins‐larvae, called penultimate Higgins‐larvae, or in the sediment. The three types of Higgins‐larvae from the Faroe Bank can be distinguished by characters such as anterior setae, posterior setae and toes. The adults of Rugiloricus bacatus sp. nov. are characterised by a prominent ruff resembling a pearl necklace; two of the eight clavoscalids are modified in the 1st row; the 2nd row of leg‐shaped scalids are very large and robust, and the 9th row with 30 beak‐like scalids alternating with 30 alternating plates. The postlarvae are free‐living and their scalids on the introvert are reduced to protoscalids. Postlarvae and adult stages have not been found for Rugiloricus sp. nov. A and B and therefore only diagnoses of these two species are presented here.

First time discovery of Loricifera from Australian waters and marine caves

Abstract Two new species of Loricifera, Pliciloricus cavernicola sp. nov. and Australoricus oculatus gen. nov. et sp. nov., have been found in two submarine caves, Jims Cave and Fish Rock Cave, off the coast of New South Wales, Australia. This is the first discovery of Loricifera from Australia and additionally from marine caves. This paper is the third paper concerning the meiofauna animals from the two caves. Pliciloricus cavernicola sp. nov. is characterized by an adult having a large tripartite mouth cone with six oral stylets; clavoscalids with fine lines; a short, robust double organ; small leg-shaped scalids with three stiff hairs; simple claw-shaped scalids; reduction of trichoscalid basal plates in the first two rows and a midventral plica with three ridges. Australoricus oculatus gen. nov. et sp. nov. is characterized by a Higgins-larva having a pair of pigmented eyes; the 2nd scalid row missing; six smooth and long filiform scalids in the 6th row; six rectangular plates with two teeth in the 7th row; three pairs of ventral setae; two large lateral lorica plates; three pairs of posterior setae and toes with balloon-shaped mucrones.