RECALLING SHUKER'S LORICIFERAN – MY VERY OWN MINI-BEAST

Caroline Gast's exquisite illustration of Pliciloricus enigmaticus, a close relative of Shuker's loriciferan P. shukeri (public domain)

Eleven years ago, I was very honoured to receive what must surely be the greatest personal accolade for any zoologist – a new species of animal was named after me. The creature in question is Shuker's loriciferan Pliciloricus shukeri – but how and why did this come about, and what exactly is a loriciferan anyway?

Although these creatures are only tiny in size, from a taxonomic standpoint the discovery of loriciferans was one of the most significant events of the entire 20^th Century, because they added a totally new phylum to the officially recognised roster of animal life. Excerpted and expanded from my book The Encyclopaedia of New and Rediscovered Animals (2012), here is their fascinating history, including the scientific debut in 2005 of P. shukeri.

My three books on new and rediscovered animals (© Dr Karl Shuker)

Loricifera - a Prediction Come True

Giving one's name to an uncommonly ugly form of animal larva may not be everyone's idea of obtaining scientific immortality, but it is nonetheless an effective way to achieve this - especially when that larva's species is so utterly different from all others that a completely new phylum has to be created to accommodate it.

Its story began in 1961 when, as a student at Washington's National Museum of Natural History, Robert P. Higgins predicted the existence of a remarkable little creature unlike any known to science at that time. By a sadistically ironic twist of fate, in May 1974 he actually found a real-life specimen of his hitherto-hypothetical creature - but failed to recognise it for what it was! Instead, he deemed it to be nothing more than a larval priapulid worm.

The following year, however, another specimen was found, this time by Danish zoologist Dr Reinhardt Møbjerg Kristensen, from the University of Copenhagen. Yet as bad luck would have it, the tiny animal was destroyed during its preparation for transmission electron microscopy. Happily, between 1976 and 1979 Dr Kristensen discovered some larvae, in shell gravel obtained from depths of 330-365 ft outside western Greenland's Godhavn Harbour. And finally, in April 1982, an adult turned up - completely by accident.

Ventral view of adult female loriciferan Nanaloricus mysticus (After R. M. Kristensen, 1983, 'Loricifera, a new phylum with Aschelminthes characters from the meiobenthus', Z. Zool. Syst. Evolutionsforsch., 21(3): 163–180)

Kristensen had obtained a huge sample of shell gravel from a depth of 83-100 ft during field work at the Marine Biological Station in Roscoff, France, and was in a hurry to examine the minute creatures living between the gravel particles, as this was his last day there before leaving for Denmark again. Consequently, instead of employing the usual sophisticated but somewhat protracted techniques for dislodging animals from the particles, lack of sufficient time spurred him to use a cruder but much quicker method - simply washing the gravel in freshwater.

The change in salt concentration experienced by the tiny marine organisms in the gravel shocked them into loosening their grip on its particles, and they could then be collected in the surrounding water. Among the creatures obtained in this way was an adult of Higgins's postulated animal form, plus others from every stage in its life history. Shortly afterwards, specimens belonging to a slightly different species were obtained from Greenland gravel samples, using this same technique.

By now, Kristensen and Higgins had learnt about each other's interest in these mysterious minute creatures, and had teamed up to work on them. They discovered that the individual (a larva) collected by Higgins in 1974 was indeed of the same group, but sufficiently different from Kristensen's species to warrant separation within a new genus and family. As for the creatures in toto, true to Higgins's expectations they required a brand new phylum. In 1983, Kristensen named it Loricifera, and formally described its first species, the Roscoff one, which he christened Nanaloricus mysticus.

Scanning electron micrograph of two Nanaloricus mysticus Higgins larvae; scale bar = 100 μm (© Dr Reinhardt M. Kristensen)

A tiny creature, no more than 0.01 in long, with a fairly squat body and a head section bearing a collar of radiating spines, it leads a sedentary existence - quite unlike its free-swimming larva, whose striated, pear-shaped body has a rear pair of flipper-like appendages. Anatomically, the species combines features from several different phyla, but is characterised by a unique mouth, consisting of a long tube that can be retracted completely within the creature's body in a manner not previously recorded from any other type of animal.

As for Higgins, although he did not have the honour of describing the first real-life species of his conjectured creature he was given an unusual consolation prize - ever afterwards, the basic larval type produced by loriciferans would be officially referred to in zoological parlance as the Higgins larva. Higgins's reaction to this accolade was to comment: “I'm very pleased of course, even though it is such an ugly creature”. Twenty-two years after his student prognostication, his hypothetical animal was hypothetical no longer.

Incidentally, in 1986 Higgins was able to describe the species to which his lost specimen had belonged; its scientific name is Pliciloricus enigmaticus, and it was just one of eight new species that Higgins and Kristensen described within a single paper. The other seven species were: P. dubius, P. gracilis, P. orphanus, P. profundus, Rugiloricus carolinensis, R. cauliculus, and R. ornatus. In 1988, Kristensen described a notably important species, P. hadalis - the first loriciferan recorded from fine sediment (red clay), from a depth (27,082 ft) great enough to be included within the hadal bathymetric zone, and from the western Pacific.

Shuker's loriciferan Pliciloricus shukeri; scale bar = 200 μm (© Dr Reinhardt M. Kristensen)

Loriciferans possess five distinct body regions - the mouth cone, consisting of a small terminal mouth; the head (introvert), containing the brain; the neck; and a trunk portion that is in turn divided into the thorax and the abdomen. The abdomen is surrounded by a series of plates yielding a corset-like or girdle-like arrangement known as the lorica (from which they derive their zoological name, and also the vernacular name 'girdle wearers'), which is variously cuticular or highly folded in form. On their head, they bear several whorls of protective spines called scalids (earning them a second, rarely-used vernacular name - 'brush-heads'), and because adult loriciferans can withdraw their head into their neck, and their neck in turn into their trunk, when they do so it means that their head is then entirely protected by the lorica laterally and the scalids dorsally (which stick outwards). Although they do possess a body cavity, it is not a true one lined completely by mesoderm tissue (i.e. a coelom), but is one that is only partly mesoderm-lined (i.e. a pseudocoelom). They entirely lack a circulatory system and a respiratory system, but they do possess a straight-through gut from proximal mouth to distal anus, and also a well-developed nervous system. The sexes are separate (males and females), each of which possesses a single pair of gonads.

Morphologically, loriciferans share affinities with two phyla of superficially worm-like creatures - the priapulids and the kinorhynchs, and have been traditionally grouped with them in a clade known as Scalidophora. More recently, however, molecular studies have promoted a closer taxonomic affinity between Loricifera and Nematomorpha (the latter phylum containing the horsehair worms).

In February 1992, I was delighted and honoured to learn from Dr Kristensen that in due course he would be naming a new species of loriciferan after me (at that time, he had nearly 70 undescribed species in his collection!), in recognition of the very significant contribution made to the zoological literature by my first book on new and rediscovered animals – The Lost Ark: New and Rediscovered Animals of the 20th Century (1993). He later informed me that 'my' loriciferan was currently the most interesting species known, because it is neotenous, i.e. its Higgins larval stage becomes sexually mature precociously, developing an ovary, so the post-larval stage is reduced. Also, it was the first loriciferan species known to possess a double secondary organ, and was markedly different from all previously-described Pliciloricus species, thereby requiring the diagnosis of the genus Pliciloricus to be amended accordingly.

Schematic diagram of the adult, type specimen of P. shukeri from Heiner and Kristensen, 2005 (© Drs Iben Heiner and Reinhardt M. Kristensen)

Three specimens of Shuker's loriciferan (one 210-μm-long adult, serving as the holotype or type specimen, and two smaller Higgins larvae, serving as paratypes) had been collected at BIOFAR (Benthic Investigation of the Faroe Islands) Station 627 on the Faroe Bank by the German research vessel Valdivia in 1990, and their species was formally described by Kristensen and fellow loriciferan researcher Dr Iben Heiner in 2005, when it was duly christened Pliciloricus shukeri. Quoting from their paper, the etymological derivation of this species’ name is as follows:

The name of this species epithet is in honor of Dr. Karl Shuker, a prominent expert in cryptozoology. The new species is dedicated to Dr. Shuker for his outstanding book “The Lost Ark, New and Rediscovered Animals of the 20^th Century”. In this book, the discovery of Loricifera received much credit as one of the major events of the 20^th Century.

The full reference to the paper in which P. shukeri is formally named and described, and which should be accessed for the entire, highly-detailed morphological description of 'my' species, is:

HEINER, I. and KRISTENSEN, R.M. (2005). Two new species of the genus Pliciloricus (Loricifera, Pliciloricidae) from the Faroe Bank, North Atlantic. Zoologischer Anzeiger, 243(3): 121-138.

(The other new loriciferan species described by them in the above paper was P. leocaudatus, the 'lion-tailed loriciferan'.)

Schematic diagram of one of the Higgins larva paratypes of P. shukeri from Heiner and Kristensen, 2005 (© Drs Iben Heiner and Reinhardt M. Kristensen)

Currently (as of August 2017), 37 species of loriciferan in nine genera have been described, but at least a hundred more have been discovered and are currently awaiting description. Indeed, with delicious irony in view of their only very recent arrival in the annals of zoological discovery, based upon the findings of studies conducted so far the loriciferans appear to be one of the most abundant groups of meiofauna in the deep sea (meiofauna being tiny organisms inhabiting the spaces between sediment particles and smaller in body size than macrofauna but bigger than microfauna), they have also been shown to occur in mud on shallower water, and they may actually be one of the dominant meiofauna groups .

Moreover, in April 2010 the existence of a trio of loriciferan species inhabiting the sediments at the bottom of the L'Atalante basin in the Mediterranean Sea, over 10,000 ft deep, was formally documented in a paper (click here to access it) authored by a team of researchers that once again included Drs Kristensen and Heiner, and which was published in the scientific journal BMC Biology. This revelation was of great zoological notability, because these three loriciferan species (respectively constituting a new Pliciloricus species, a new Rugiloricus species, and a new Spinoloricus species) were the first multicellular organisms known to spend their entire lives in an anoxic or anaerobic (oxygen-free) environment.

They can achieve this remarkable feat because they utilise hydrogenosomes (or similar organelles) rather than mitochondria for providing energy. Less than 0.04 in (1 mm) long, these very specialised loriciferans undergo their life cycles in the total absence not only of oxygen but also of light.

Light microscopy image of the new species of anoxic Spinoloricus loriciferan, stained with Rose Bengal; scale bar = 50 μm (© Roberto Danavaro et al., 2010/Wikipedia CC BY 2.0 licence)

Despite having been formally known to science for over three decades now, the loriciferans have clearly lost none of their capacity to surprise the zoological world!

My sincere thanks to Dr Reinhardt M. Kristensen for most kindly making available to me for use in my writings his illustrations included here – and, above all else, for doing me the immense honour of naming a new species after me, something that I'd always dreamed about since a very small child but never expected to happen. Sometimes, dreams really do come true.

And who knows, perhaps one day a second, closely-related, but presently-unfulfilled dream of mine will also come true – that someone will also name a new species after my late mother, Mary Shuker (without whose love, guidance, and encouragement I would never have achieved anything, including writing The Lost Ark and my other books), so that her name will very deservedly live on, and that she will therefore continue to be remembered when I am no longer here to do so.  God bless you Mom, I love you and miss you so much.

Shuker's loriciferan (© Dr Reinhardt M. Kristensen)