Loricifera

(Girdle wearers)

Phylum Loricifera

Number of families 2

Thumbnail description
Group of microscopic, bilateral symmetrical animals characterized by a body with five sections: a protrusive mouth cone; a head (introvert) with up to nine rows of scalids (in the adults); a neck with trichoscalids; a thorax; and an abdomen with a lorica consisting of plates or plicae (folds)

Evolution and systematics

Loricifera is traditionally considered a phylum in the group Introverta. The closest relatives of the loriciferans are the Kinorhyncha (kinorhynchs) and Priapulida (priapulans). Loricifera includes 11 described species as of 2003. All species have been assigned to one order named Nanaloricida that includes two families, the Nanaloricidae and the Pliciloricidae. As of 2003, more than 100 species have been collected that have not yet been described.

Physical characteristics

Adult loriciferans range in size from 0.008 to 0.0157 in (200–400 µm). The largest specimen ever recorded was a giant larva from the deep sea that measured about 0.027 in (700 µm). The body is divided into five sections: a mouth cone; a head that can be introverted or drawn into the body; a neck; a thorax; and an abdomen. The mouth cone consists of 6–16 oral ridges and a cuticulanized, extrudable buccal tube. Furthermore, some nanaloricids may have six oral stylets.

The head, or introvert, consists of nine rows of sensory or locomotory structures called scalids. The scalids in the first row are called clavoscalids whereas the scalids in the remaining eight rows are called spinoscalids. There are usually eight clavoscalids; however, males of the family Nanaloricidae always have more clavoscalids than the females. The second and third rows of scalids vary greatly in the number of scalids in each row (from 7–15) and types. There are different kinds of leg-shaped scalids and a ventral double organ. The number of scalids in the fourth through the eighth rows is always 30. In the fourth row, the scalids may alternate between the typical spinoscalids and a noticeable claw-shaped variation on the typical form. The spinoscalids in the fifth through the seventh rows always belong to the common, simple type. The spinoscalids in the eighth row resemble the trichoscalids of the neck region; sometimes they have alternating plates. The scalids in the ninth row in pliciloricids have beak-like structures. These scalids are not present in nanaloricids.

The neck of loriciferans consists of three rows of plates with 15 plates in each row and 15 appendages known as trichoscalids. The trichoscalids are flattened with serrated margins; they either alternate between eight single and seven double scalids or have 15 single trichoscalids. The thorax has no appendages. The abdomen consists of a lorica with either 6–10 strong cuticularized plates or 22–40 plicae. A varying number of sense organs are present toward the rear of the abdomen. These specialized receptors are called flosculi and can be divided into two types; Nanaloricus-flosculi and Pliciloricus-flosculi.

Internally the body consists of a pharynx bulb, a digestive system with a short esophagus, and a straight midgut. The reproductive system consists of a pair of sack-shaped gonads with a pair of protonephridia, or primitive excretory organs, inside the gonads. The protonephridia are divided into anterior and posterior parts. Their presence inside the gonads is unique to Loricifera. In addition to these organ systems, the body of loriciferans contains a complex muscular system as well as a nervous system with a large brain and ventral nerve cord with ganglia (groups of nerve cells located outside the brain).

The postlarvae in the family Nanaloricidae look like adults although they lack one row of scalids and a reproductive system. The postlarvae in the family Pliciloricidae, however, differ significantly from the adults because their scalids are reduced in size and much simpler in appearance.

The Higgins larva ranges in size from 0.003–0.0197 to 0.027 in (80–500 to 700 µm) and is easily recognized by the presence of two conspicuous toes. It is named for Professor Robert P. Higgins in honor of his longtime study of the Introverta. The body of the Higgins larva is divided into the same sections as the adult. The mouth cone consists of either 6–12 double oral stylets (thin rods) and/or six oral ridges. The head, or introvert, consists of seven rows of scalids with eight clavoscalids in the first row. The second through the seventh row have spinoscalids as in the adult. The bilateral symmetry is pronounced in the arrangement of the larval scalids. The neck sometimes has a collar-like area that can close over the introvert when it is retracted into the body. The thorax resembles an accordion, having 5–6 ventral longitudinal folds. The abdomen also has longitudinal folds, but only on its sides and dorsal surface. Two or three pairs of sensory or locomotory setae (bristles) are located on the larva's ventral surface in the area between the thorax and the abdomen, with two or three pairs of setae and a pair of toes located toward the rear of the lorica. The toes are used for movement and have adhesive glands. There are several flosculi of the Nanaloricus-type on the abdomen of the Higgins larva.

Distribution

As of 2003, information is limited regarding the distribution of Loricifera. Representative organisms from this group have been recorded in relatively few locations. It is very likely, however, that these records reflect the scarcity of sampling rather than the actual distribution of loriciferans. The group is probably present in the marine meiofauna throughout the world, from shallow to deep coastal and abyssal waters. Meiofauna refers to a category of microorganisms that are large enough to see with a basic microscope but too small to see with the naked eye. Loriciferans have been sampled in the coastal waters of France, Denmark, and North Carolina (USA); the Faroe Islands of the North Atlantic; the Mediterranean; the Coral Sea off Queensland, Australia; the Angola basin in the southeastern Atlantic; and from the Great Meteor Seamount in the North Atlantic. They have been sampled in abyssal waters in the Gulf of Mexico at a depth of 9,708 ft (2,959 m) and the Izu-Ogasawara trench at a depth of 27,100 ft (8,260 m) off Japan. Loriciferans are common in polar waters, especially in the deep sea.

Habitat

Loriciferans are found exclusively in marine habitats, and live in the spaces between sand grains or in the mud at the bottom of the deep sea. The nanaloricids prefer sand with low levels of detritus (material derived from the decomposition of once-living organisms) or clean shell gravel, whereas the pliciloricids are often found in such deep-sea sediments as the white abyssal Globigerina ooze and the red deep-sea clay from the hadal zone (below 20,000 ft; 6,100 m). Both families of Loricifera have been recorded in Australian marine caves, and a new nanaloricid genus was discovered in 1998 in sediments influenced by hydrothermal vents in the deep waters of the Kilinailau Trench off Papua New Guinea.

Behavior

Studies of loriciferan behavior are extremely scarce since most of the animals die before they can be examined. They have been studied live a few times, however, and researchers have observed their movement patterns and mating behavior.

The adults and the larvae both adhere strongly to the sediment with a kind of glue made by the adhesive glands located toward the rear of the adults and on the toes of the larvae. The adults usually crawl by using their many scalids and their mouth cones. Observers have noticed that the mouth cone telescopes out to its full length, fastens itself to a sand grain, and then draws in again so that the loriciferan's body is pulled forward.

The larvae may use their scalids and setae to crawl between grains of sand. They can also swim by using their toes. Larvae of the family Nanaloricidae, whose members have large and flipper-shaped toes, have sometimes have been found swimming free among the plankton. The larvae of the family Pliciloricidae have thin spine-shaped toes and are probably unable to swim; their movement is apparently restricted to crawling.

Little is known about the mating behavior of loriciferans. It is assumed, however, that the branched clavoscalids in the males of the family Nanaloricidae are used as chemoreceptors to locate female sex pheromones. The males in this family also have one ventral modified hook-shaped pair of trichoscalids that hold the female during copulation.

Feeding ecology and diet

Loriciferans probably feed on suspended organic particles, microalgae, and bacteria. They eat bacteria or algae by piercing them with their oral stylets and then sucking out the contents. The spinoscalids of nanaloricids are often completely covered with bacteria. It is still uncertain why the bacteria are present in such numbers. Some researchers suggest that the animals collect the bacteria from the interstitial water, whereas others maintain that the animals cultivate the bacteria on the mucus that they secrete. What is certain is that the loriciferans feed on these bacteria; this is confirmed by the fact that their digestive tracts are filled in some cases with partially digested bacteria.

Reproductive biology

Loricifera have very complicated life cycles with both sexual and asexual forms of reproduction. Members of the family Nanaloricidae reproduce only sexually and have distinct sexual dimorphism; that is, different body forms related to gender. The dimorphism is illustrated in the males by some of the clavo- and trichoscalids that are modified pheromone receptors as well as hooks to hold the female during copulation. Fertilization may be either internal or external. The primary larva, the Higgins larva, hatches from the fertilized egg and grows by molting. After at least 2–5 larval instars (stages between molts), the larva metamorphoses into a postlarva. The postlarva is a dormant stage and never feeds. A male or female with fully developed gonads emerges from the postlarva and the life cycle repeats itself.

The members of the family Pliciloricidae follow two different life cycles, named the Rugiloricus cauliculus and Rugiloricus carolinensis cycles respectively. The Rugiloricus cauliculus cycle includes a cycle of sexual reproduction like the one in the family Nanaloricidae. The only difference is that the postlarva looks different from the adult. The scalids of the postlarva are reduced in size and much simpler in form. The Rugiloricus cauliculus cycle, however, also comprises an asexual cycle in which the Higgins larva develops a mature ovary. The maturation of larval ovary is usually called neoteny, hence the matured larval stage is named the neotenous larva. Several (4–8) Higgins larvae form inside the neotenous larva. The larvae are formed by parthenogenesis, which means that they develop from female gametes without fertilization and are therefore genetically identical to the neotenous larva. The parthenogenetic larvae are completely identical to the Higgins larva and may develop either into new neotenous larvae or into a postlarva that will molt later into an adult male or female.

In the Rugiloricus carolinensis cycle, the postlarva is reduced so that only the cuticle of the postlarva is left inside the larva. The adult then emerges directly from the larva. Several reductions occur in the life cycle of an undescribed order from the Faroe Islands in the North Atlantic. The cuticles of the postlarva and the adult are found inside a cyst-like larva, and a mature ovary with several eggs develops inside these cuticles. The eggs mature into normal Higgins larvae that eat the maternal individual. The new larvae emerge from an opening in the rear of the empty exuvium (cast-off covering) of the cyst-like larva. This mode of reproduction is called pedogenesis and is usually seen only in nematodes and insects.

Conservation status

No species of loriciferans are listed by the IUCN.

Significance to humans

Loriciferans may have some significance to humans. They are found in large numbers in areas where methane seeps from the sediment. It may be possible in the future to use loriciferans or other meiofauna as indicators for the presence of methane or other gases.

Species accounts

List of Species

French girdle wearer

Nanaloricus mysticus

order

Nanaloricida

family

Nanaloricidae

taxonomy

Nanaloricus mysticus Kristensen, 1983, off the coast of Roscoff, France.

other common names

None known.

physical characteristics

The adults measure 0.00894–0.00925 in (227–235 µm). The mouth cone has eight oral ridges. The introvert has eight rows of true scalids; however, the first row of tricoscalid plates is fused with a row of scalids, giving the impression of a ninth row. Both sexes have eight clavoscalids. The male's clavoscalids are all branched except for the midventral pair, which resembles the female's clavoscalids. The last two rows on the introvert are beak-or tooth-like scalids. The lorica consists of six plates with a fine honeycomb structure. Flosculi are present in two pairs on the plates along the back and sides, and as a single flosculum on the anal plate.

The Higgins larvae measure 0.0047–0.0072 in (120–185 µm). The mouth cone lacks an armature (protective structure). The introvert has seven rows of scalids. The accordion-like thorax consists of 5–6 folds. Three ventral pairs of setae are located between the thorax and the abdomen. The lorica has coarse honeycomb ornamentation. Three pairs of anterior setae are modified to form a locomotory organ with grasping function. Three pairs of posterior setae are located on the lorica together with a pair of toes. The toes are flattened by a leaf-like structure called the mucro.

distribution

Roscoff, France. Two previously published records from Florida and the Azores Islands respectively turned out to refer to two undescribed species.

habitat

Found in the upper surface layer of Dentalium-sand (a specific type of coarse sand with high concentrations of detritus) at a depth of 65.6–82 ft (20–25 m).

behavior

The Higgins larva may be able to swim by using its large leaf-like toes as a propeller.

feeding ecology and diet

In the first description of the Loricifera, it was postulated that this species is ectoparasitic because one specimen was attached

to a copepod. This finding, however, turned out to be an artifact, or misleading result arising from the way the specimen was prepared. Nanaloricids feed exclusively on bacteria.

reproductive biology

Sexual reproduction.

conservation status

Not listed by the IUCN.

significance to humans

None known.

Japanese deep-sea girdle wearer

Pliciloricus hadalis

order

Nanaloricida

family

Pliciloricidae

taxonomy

Pliciloricus hadalis Kristensen & Shirayama, 1988, Izu-Ogasawara Trench, Western Pacific.

other common names

None known.

physical characteristics

Adults measure 0.0058–0.0086 in (149–219 µm). The males are smaller than the females. Mouth cone is small and without mouth tube. The leg-shaped scalids in the second row are very large and robust. Two of the scalids in the second row are modified into a short and thick double organ. The fourth row has 15 claw-shaped scalids and 15 simple spinoscalids. The trichoscalids (eight single and seven double) are very long, about 0.0039 in (100 µm). The abdomen consists of 20 plicae. A single pair of Pliciloricus-flosculi is located caudally. Higgins larvae are long and slender, measuring 0.0103 in (262 µm). There are seven rows of scalids. The spinoscalids are long, over 0.00197 in (50 µm). Two pairs of setae are situated between the thorax and the abdomen. The toes are very long, about 0.006 in (153 µm), straight and pointed. Three pairs of setae are located toward the rear of the abdomen.

distribution

The hadal bathymetric zone of the deep sea (below 20,000 ft; 6,100 m). Found in the Izu-Ogasawara Trench off Japan at a depth of 27,100 ft (8,260 m).

habitat

Red deep-sea clay.

behavior

One specimen was found 1.57 in (4 cm) deep in the clay, which indicates that the animal is capable of burrowing or living in association with a tube-dwelling macrofauna animal.

feeding ecology and diet

Probably bacteria.

reproductive biology

The mode of reproduction of this species is not understood. The lack of seminal receptacles in the female suggests that this species has external fertilization.

conservation status

Not listed by the IUCN.

significance to humans

None known.

Bucket-tailed loriciferan

Rugiloricus cauliculus

order

Nanaloricida

family

Pliciloricidae

taxonomy

Rugiloricus cauliculus Higgins & Kristensen, 1986, off the coast of South Carolina, United States.

other common names

None known.

physical characteristics

Adults measure 0.0071–0.0103 in (180–264 µm). Mouth cone is very small. Introvert with nine rows of scalids. Appearance of the clavoscalids displays sexual dimorphism. Two types of clavoscalids (four large dorsal and four small ventral) are present in the male, but not in the female. The fourth row has 15 claw-shaped scalids and 15 simple spinoscalids. Lorica has 60 plicae. Anal cone pointed. The larvae measure 0.0108 in (275 µm), but are insufficiently described.

distribution

Found on the continental shelf off North and South Carolina, USA; in the Mediterranean Sea; and near the Faroe Islands. The identity of the Faroe Islands specimens is slightly uncertain, however; they may represent a new species.

habitat

Coarse phosphorite or oolytic sand at a depth of 656–1,640 ft (200–500 m).

behavior

Nothing is known.

feeding ecology and diet

Probably feeds exclusively on methano-bacteria.

reproductive biology

Sexual and asexual life cycles, including parthenogenesis with neotenous larvae (see Reproductive behavior in main chapter).

conservation status

Not listed by the IUCN.

significance to humans

None known.

American diamond girdle wearer

Rugiloricus carolinensis

order

Nanaloricida

family

Pliciloricidae

taxonomy

Rugiloricus carolinensis Higgins & Kristensen, 1986, South Carolina, United States.

other common names

None known.

physical characteristics

Adults measure 0.008 in (205 µm). Introvert has nine rows of scalids. The clavoscalids in the first row are all uniform. The second row has between 9–15 leg-shaped spinoscalids. The fourth row has 30 uniform spinoscalids. The neck region consists of 15 single trichoscalids. The lorica consists of 30 plicae with a pair of Pliciloricus-flosculi and a large anal field.

distribution

Found on the continental shelf off North and South Carolina, USA, and near the Faroe Islands in the North Atlantic. The specimens from the Faroe Islands may be a new species.

habitat

Coarse phosphorite and carbonate sand.

behavior

The Higgins larvae may have a very patchy distribution. More than 200 larvae were collected in one sample in phosphorite sand at a depth of 964 ft (294 m) east of Cape Romain, South Carolina.

feeding ecology and diet

Feeds on microalgae and bacteria.

reproductive biology

Sexual reproduction with reduced postlarvae. The postlarval stage is very short and the cuticle consists only of a thin membrane without scalids. Therefore, it looks as if the Higgins larva molts directly into a mature adult. This species may also have an asexual life cycle with parthenogenetic neotenous larvae.

conservation status

Not listed by the IUCN.

significance to humans

None known.

Resources

Books

Kristensen, Reinhardt M. "Loricifera." In Microscopic Anatomy of Invertebrates. Vol. 4, Aschelminthes, edited by F. W. Harrison and E. E. Ruppert. New York: Wiley-Liss, 1991.

Periodicals

Higgins, R. P., and R. M. Kristensen. "New Loricifera from Southeastern United States Costal Waters." Smithsonian Contributions to Zoology 438 (1986): 1–70.

Kristensen, R. M. "Loricifera, A New Phylum with Aschelminthes Characters from the Meiobenthos." Zeitschrift für Zoologische Systematik und Evolutionsforschung 21 (1983): 163–180.

——. "An Introduction to Loricifera, Cycliophora, and Micrognathozoa." Integrative and Comparative Biology 42 (2002): 641–651.

Kristensen, R. M., and Y. Shirayama. "Pliciloricus hadalis (Pliciloricidae), A New Loriciferan Species Collected from the Izu-Ogasawara Trench, Western Pacific." Zoological Science 5 (1988): 875–881.

Todaro, M. A., and R. M. Kristensen. "A New Species and First Report of the Genus Nanaloricus (Loricifera, Nanaloricida, Nanaloricidae) from the Mediterranean Sea." Italian Journal of Zoology 65 (1998): 219–226.

Iben Heiner, MSc

Martin Vinther Sørensen, PhD

Reinhardt Møbjerg Kristensen, PhD