Micrognathozoa (Jaw Animals)
Number of families 1
Microscopic animal group with one described species, Limnognathia maerski, characterized by the presence of intracellular plates in the dorsal and lateral epidermis; the ventral epidermis is covered with frontal and ventral ciliation (ciliophores); sensory structures consist of serially arranged tactile bristles; the digestive system has a highly complex jaw apparatus, a simple midgut, and a dorsal, periodically functioning anus
Evolution and systematics
Micrognathozoa contains only a single species, Limnognathia maerski, which was discovered in 1994 but first described in 2000 by R. M. Kristensen and P. Funch. It was cited as a new class, but owing to its numerous unique character traits, it could not be assigned to any known phylum. The special morphological features of its integument and the presence of a complex jaw apparatus, however, pointed toward a close relationship with the Rotifera, and Micrognathozoa therefore were assigned to the superphylum Gnathifera (that is, "those that possess jaws"), which, besides the Rotifera, contains the phyla Gnathostomulida (jaw worms) and Acanthocephala (thorny-headed worms). The phylum Micrognathozoa contains one class, Micrognathozoa; one order, Limnognathida; and one family, Limnognathiidae.
The taxonomy for this species is Limnognathia maerski Kristensen and Funch, 2000, Disko Island, Greenland.
Limnognathia maerski is a microscopic, acoelomate animal that ranges in size from 0.004 to 0.006 in (100–150 µm). Its body is divided into a head, an accordion-like thorax, and an abdomen. The dorsal and lateral parts of the integument have no ciliation, except scattered sensory bristles that are made up of joined cilia. The epidermis consists of several epidermal plates, and each plate is made up of two to four epidermal cells. It lacks a true cuticle, and the only cover is a very thin glycocalyx. Instead of an extracellular cuticle, it has a filamentous intracellular lamina that helps make the integument stiffer. Most of the ventral part of the integument lacks both cuticle and the intracellular lamina; instead, it has a much thicker extracellular glycocalyx. It does have one large cuticular area, called the oral plate, posterior to the mouth opening. Most of the ventral side is covered with cilia that are arranged in four distinct groups.
The frontal part of the head has bands of cilia that beat metachronously (using coordinated waves) and resemble those found in Rotifera and various protostome larvae. On each side of the oral plate there are four groups of cilia. The cilia in each group beat in unison, and all cilia arise from a single cell, a so-called ciliophore. The ventral side of the thorax and abdomen is covered by a dense mat of cilia that arise from a double row of ciliophores. The fourth group of cilia is located on the caudal part of the abdomen and is formed by cilia that arise from an adhesive pad that consists of ten cells.
The mouth is located ventrally, anterior to the oral plate, and leads to the pharynx, which contains a highly complex jaw apparatus. It consist of several independent elements that are interconnected by ligaments and fine, cross-striated muscles. The central part of the jaws consists of the large main jaws that anteriorly form a pair of forceps with long teeth. A pair of large droplet-shaped elements, the fibularia, are located lateral to the main jaws, and two cuticular bridges, named the reinforced web, connect the anterior parts of the fibularium with the forceps of the main jaw. A pair of rodshaped elements with distal teeth is located on the dorsal side of the fibularium. These elements are called the dorsal jaws. A cuticular membrane covers the ventral side of the main jaw and fibularium, and ventrally on this membrane other elements are present, including the oral lamellae, the ventral jaws and the basal plates. If the jaw elements are investigated with scanning or transmission electron microscopy, they can be seen to be composed of extremely fine, rodlike fibrillae, and this is identical to the ultrastructure in the jaws of Rotifera (wheel animalcules) and Gnathostomulida (jaw worms), hence supporting a close relationship between these groups.
A short esophagus leads to the gut and then to the rectum. A normal, permanent anus apparently is lacking. Instead, the rectum gradually narrows and at its terminus, near the integument, is blocked by an anal plate. The anal plate has a pair of small muscles, which suggests that it can be moved so that the anus becomes periodically functional. However, defecation has never been observed. Two pairs of protonephridia control excretion and maintenance of osmotic balance. The protonephridial terminal cells are monociliated, contrary to all other ciliated cells in L. maerski.
Micrognathozoans have a bipolar distribution. Limnognathia maerski was found in the cold Isunngua spring at the bay of Aqajarua (Muddy Bay) on the northeastern part of Disko Island, western Greenland, in the summer of 1994. Since its discovery, several hundred specimens have been collected from this spring, but recordings from nearby springs are very few. Three specimens from a collection made in 1979 from a spring close to Lymnaea Lake in the valley of Sullorsuaq/Kvandalen (Angelica Valley) were rediscovered in 1995. Lymnaea Lake is located about 10.5 mi (17 km) from the Isunngua spring. In 1997 the species was collected from different freshwater bodies on the Crozet Islands, located between Africa and Australia, 1,500 mi (2,400 km) north of Antarctica. It has not been determined how the species has this peculiar distribution, but one explanation could be that L. maerski has very narrowly defined demands in terms of habitat and climate and that such localities still are poorly investigated. The search for L. maerski has been intense in all kinds of homothermic springs (those with a constant temperature throughout the year) as well as heterothermic springs (those that may freeze in the winter) throughout the world, without any further findings.
Limnognathia maerski lives in mosses in running or stagnant freshwater, but it also may inhabit sandy bottom sediments. Knowledge of its ecology is extremely limited, but the distribution suggests that it prefers low-temperature waters. On Disko Island it has been found only in cold springs that often are frozen for seven to eight months of the year. The adult animals cannot survive freezing, but it is likely that their thick-shelled resting eggs (see Reproductive biology) can tolerate such extreme conditions. Interestingly, Disko Island has more than a thousand homothermic springs that maintain a constant temperature throughout the year and therefore also run during the winter, but L. maerski clearly avoids this kind of spring, which suggests that the deep-frozen period is important for its life cycle.
When L. maerski moves, it either crawls or swims. While swimming, it moves slowly in a characteristic spiral, which makes it easy to distinguish from other microinvertebrates. The swimming motion is created by the ventral trunk ciliophores; hence, the ciliary bands in the head are not involved in locomotion. When crawling, it also uses ventral ciliophores and glides slowly on the substratum. This slow gliding very much resembles the movement of chaetonotid gastrotrichs
and the microscopic polychaete Diurodrilus. If a crawling individual is disturbed, it stops and adheres strongly to the sub-stratum with the ventral adhesive pad.
Feeding ecology and diet
Limnognathia maerski feeds on bacteria, blue-green algae, and diatoms. During the search for food the head moves slowly from side to side while the ciliary bands on the head beat food particles toward the mouth. When a food item reaches the mouth, it is quickly grabbed by the ventral jaws, dragged into the pharynx, and processed by the main jaws. The species appears to be highly selective in its food choice; if it by accident grabs and swallows an unwanted item, it quickly rejects it. Following its characteristic "vomit behavior," it lifts the forehead to a vertical position that pushes the whole jaw apparatus out of the mouth; while the animal stands in this position, the swallowed item is ejected.
Even though L. maerski has been sampled frequently throughout the short Arctic summer over the course of several years, male individuals have never been seen, and it is certain that reproduction is based on parthenogenesis, at least in part. The female reproductive system is rather simple and comprises a pair of ovaries. The ovaries consist mostly of oocytes, and yolk appears to be produced inside each developing egg from small molecules that diffuse through the thin shell. Oviposition can be provoked by pricking the animal gently with a thin needle or by increasing the temperature by a few degrees. The egg is laid through a small pore posterior to the ventral adhesive pad.
Limnognathia maerski is capable of producing two kinds of eggs: a thin-shelled type and a type with a much thicker, sculptured shell. The latter egg resembles the resting eggs that are produced during the sexual phase of the reproductive cycle of monogonont rotifers. If the micrognathozoan cycle can be compared to the rotiferan one, it would suggest that the thin-shelled eggs are products of asexual parthenogenetic reproduction, whereas sexual reproduction is involved in the formation of the sculptured type. Hence, males could be present, at least periodically. One possibility is that L. maerski, like rotifers, produces dwarf males that live only for a very short period and therefore have not yet been found. Another possibility is that Micrognathozoa are protandric hermaphrodites, which means that the animals hatch as males and then quickly develop into females. Both solutions are purely hypothetical.
The type locality of L. maerski is protected by the international wetlands convention (RAMSAR site). Both the bay of Aqajarua and the valley of Sullorsuaq, with the many eutrophic lakes, are important as feeding sites for numerous species of Arctic birds.
Significance to humans
Funch, Peter, and Reinhardt M. Kristensen. "Coda: The Micrognathozoa—a New Class or Phylum of Freshwater Meiofauna?" In Freshwater Meiofauna: Biology and Ecology, edited by S. D. Rundle, A. L. Robertson, and J. M. Schmid-Araya. Leiden, The Netherlands: Backhuys Publishers, 2002.
Ahlrichs, W. H. "Epidermal Ultrastructure of Seison nebaliae and Seison annulatus, and a Comparison of Epidermal Structures within the Gnathifera." Zoomorphology 117 (1997): 41–48.
De Smet, Willem H. "A New Record of Limnognathia maerski Kristensen & Funch, 2000 (Micrognathozoa) from the Subantarctic Crozet Islands, with Redescription of the Trophi." Journal of Zoology (London) 258 (2002): 381–393.
Kristensen, Reinhardt M. "An Introduction to Loricifera, Cycliophora, and Micrognathozoa." Integrative and Comparative Biology 42 no. 3 (June 2002): 641–651.
Kristensen, Reinhardt M., and Peter Funch. "Micrognathozoa: A New Class with Complicated Jaws like Those of Rotifera and Gnathostomulida." Journal of Morphology 246, no. 1 (October 2000): 1–49.
Sørensen, M. V. "Further Structures in the Jaw Apparatus of Limnognathia maerski (Micrognathozoa), with Notes on the Phylogeny of the Gnathifera." Journal of Morphology 255, no. 2 (February 2003): 131–145.
Martin Vinther Sørensen, PhD
Reinhardt Møbjerg Kristensen, PhD