Phoronids are exclusively marine animals, distributed all over the world. At present The phylum Phoronida comprises 12 described species (Emig, 1979; Temereva, Malakhov, 1999; Temereva, 2000). Adult phoronids have a vermiform body (Fig. I (1, 2)) and live in tubes excreted by themselves (Fig. II (1, 2http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">)). Tube walls are formed of hardened chitin secretion of epithelium (Hyman, 1958, 1959), they are transparent and elastic, but in some species they are incrusted and reinforced by ground grains (Fig. II (1, 2http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">)). Two ecological groups are distinguished among phoronids: burrowing and encrusting (Emig, 1982, 1985). The former ones settle in mollusk shells (Acmaea, Niveotectura, Chlamys, Crassostrea, Crenomytilus, Fusitriton) and in rocks, and the latter ones – in sand, and their tubes are incrusted with grains of sand (Fig. I (2)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">; IIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
Animal body is fully buried in a tube, and only head end of the body with lophophore tentacles looks out into water (Fig. I (2)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">; II (4, 5)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Body length is always shorter than the tube length and varies greatly both within one species and among species, it may range from 1.5 cm (Phoronis ovalis) to 45 cm (Phoronopsis californica). Living animal body color may be milk-white, rose-tinted, greenish or brown.
Outwardly body of all phoronids can be subdivided into five sections: lophophore with tentacles, head section of the body, anterior and posterior body sections and ampulla (Temereva, Malakhov, 2001) (Fig.II (1)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Head end bears lophophore, of function which is feeding and respiration. Lophophore tentacles embrace the mouth, which has a shape of falcate-curved opening and covered with the epistome (over-mouth fold). Head body part is short, and from outward anal side of the body it is designated with two metanephridium lumps (Fig. I (3)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Anterior part of the body is the longest part of phoronids body, which is characterized by a folding mantle and an ability to heavily contract, becoming almost twice shorter and drawing the head end in the tube (Fig. I (3)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Posterior body part is characterized by the largest diameter (as compared with the other body parts) and by thin semitransparent mantle, through which blood vessels and intestinal loop can be seen. Terminal body part – ampulla – is shape as a small phial and is characterized by folding mantle and the ability to change its diameter very much (Fig. II (1)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
Phoronids have oral and anal sides of the body. On the anal side the anal papilla, lumps of metanephridia and two lophphpore branches are well noticeable (Fig. I (3)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
Morphology of phoronids is very simple, and only genus can be identified by appearance. Two genera - Phoronis and Phoronopsis - are distinguished in Phoronida phylum. Representatives of Phoronopsis genus are characterized by the presence of epidermal fold – a collar, developed under the lophophore along the outer row of tentacles and surrounding circular nervous plexus. The collar is especially well visible in the binocular by sides and on the anal side of the body (Fig. I (3)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Species ofPhoronis genus lack collar.
For identification of phoronid species it is necessary to examine histological sections, made through every part of the body. At that, for the head part complete series of sections should be made. Cross sections through lophophore basis help to identify lophophore type and to count the number of tentacles which is important for species identification. Lophophore in all phoronids is bilaterally symmetrical, and its arrangement is an important taxonomic feature. Phoronids have five types of lophophore arrangement: oval, horseshoe-shaped, transitional to spiral (0.5 coil), spiral (with 1-4 coils) and helicoidal (Emig, 1979; Temereva, Malakhov, 1999) (Fig. IIIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
Continuos row of tentacles open on the anal side in most phoronids. In this region a zone of laying new tentacles (aboral formation zone) is situated, therefore the shortest tentacles are here. The only phoronid species – Phoronis muelleri – has not only aboral, but also oral formation zone (Mamkaev, 1962; Emig, 1979) (Fig. II (3)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). The latter one is situated from the oral side of the body. Here medial tentacles are twice or thrice shorter than the lateral ones (Fig. II (3)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
All elements of the nervous system of phoronids lie in the thickness of coating epithelium. The nervous system includes dorsal nerve plexus (situated between mouth and anus), circular nerve plexus (runs along the outer row of tentacles in lophophore basis), giant nerve fibers, intra-epidermal nerve plexus (Silen, 1954a). Two (right and left) or one (left) nerve fiber can be found on cross sections through the anterior body part in different phoronids species (Fig. IVhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). The number and diameter of the giant nerve fibers have a systematic significance. Nerve fibers run in the thickness of epithelium opposite the lateral mesenteries. In the most phoronids nerve fiber diameter does not exceed 10 μm (4-9 μm), and they can be found only using oil immersion lens (Fig. IV (1)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). However some phoronids have a very sizeable diameter of nerve fibers – 30-40 μm (Fig. IV (2)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
Muscles of skin-muscular sack are formed by the layer of circular and longitudinal muscles. Longitudinal muscles are the most strongly developed in the anterior part of the body, where they form folds, which jut out into the body cavity (Fig. IV (2)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Four types of longitudinal muscles are distinguished in phoronids: feathery, bushy and two types of syncytial muscles, which are specific for the only one phoronid species -Phoronis pallida (Silen, 1952) (Fig. Vhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
The number of muscular folds in separate coelom chambers is one of the main systematic features of phoronids, which was for the first time introduced in the taxonomy of this group by Selys-Longchamps (1907). The number of longitudinal muscles bands is counted by the following scheme:
oral mesentery
left lateral mesentery --|--right lateral mesentery
anal mesentery
The number of longitudinal muscles bands can be determined by sections across the anterior body part (Fig. VIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Body coelom of phoronids includes five mesenteries: oral, anal, inter-intestinal (runs between two intestinal branches) and left and right lateral ones (Fig.VIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). The first three mesenteries divide body coelom into right and left chambers. Additional lateral mesenteries divide the coelom into anal and oral chambers. In two phoronid species some of the mentioned mesenteries may be absent, what is a definitive distinction for these species. Thus, Phoronis ovalis has no both lateral mesenteries, andPhoronis muelleri – left lateral mesentery (Mamkaev, 1962; Emig, 1974, 1979).
It is very easy to determine left and right coelomic chambers in the species, having only one (always left) giant nerve fiber. Mesentery, approaching nerve fiber, is a left lateral one, then a chamber, closest to it and containing blood vessel, is left oral, and a chamber without a vessel is left anal (Fig. VIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). One more margin of the left oral chamber is accordingly an oral mesentery, and that of the left anal chamber – anal mesentery. The remaining mesentery is right lateral one, which divides the right coelom chamber into oral (adjoining oral mesentery) and anal one (adjoining anal mesentery).
It is more difficult to determine coelom chambers in species with two nerve fibers: for an inexperienced researcher it will be hard at first to understand, which mesentery, approaching nerve fibers, is right and which is left.
Generally, circulatory system of phoronids is closed and consist of several main blood vessels: two lophophoral (circular) and three longitudinal (right and left lateral, and medial). In all phoronids with one exception (Phoronis ovalis) one of three longitudinal vessels (right) is reduced along the greater body length, and only two blood vessels – left and medial - can be seen on cross sections across the middle of the body. However, in the posterior body part, where gonads are placed, there is the third longitudinal vessel (see Temereva, Malakhov, 2003). In Phoronis ovalis all three longitudinal vessels are visible on cross sections across the middle of the body.
In order to determine coelomic chambers it is necessary to clarify which of two blood vessels on the section is a medial one, and which is left lateral one. The former is closer to the inter-intestinal mesentery, and as a rule it has a narrow opening and thick walls with inner pavement (Fig.IV (1)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">; VIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). The latter is farther from the inter-intestinal mesentery, has a wide opening and thin walls (Fig. VIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Medial blood vessel is in the right anal coelomic chamber, which is limited by anal and right lateral mesenteries. The left lateral vessel runs in the left oral coelomic chamber, which is limited by oral and left lateral mesenteries. Two chambers of coelom, which have no blood vessels, are called right oral and left anal ones. The former is limited by the right lateral and oral mesenteries, and the latter – by anal and left lateral ones.
The structure of phoronids metanephridia is systematically important. They are pair organs, situated in the head part of the body in a shape of a curved tube, one end of which opens with a ciliary funnel into the cavity of the body coelom, and another end – with nephridiopore into the surroundings (Fig. VIIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Four types of metanephridial structure can be distinguished (Emig, 1979, 1985):
- with one ascending branch and one funnel (Fig. VII (1)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">);
- with one ascending branch and two funnels: large anal and small oral (Fig. VII (2)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">);
- with two branches – ascending and descending, and one funnel (Fig. VII (3)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">);
- with high nephridial branches, with nephridiopore, situated on the inner side of the anal papilla, with two funnels, from which the oral one is much greater than the anal one and has big blades (Fig.VII (4)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
It is necessary to note that coelomic funnels of metanephridia in of the most phoronid species often increase in size during spawning period and form multiple folds, blades and, probably, additional funnels. Such precedents are reliably known for Phoronis psammophila (Emig, 1985),Phoronopsis albomaculata (Emig, 1979). In order to reconstruct metanephridia should be obtained a complete series of histological sections across the head part of the body.
Among phoronids there are both dioecious and hermaphrodite species (Emig, 1977). Sexual cells develop in the posterior body part in the thickness of vasoperitoneal tissue, and are associated with blood vessels and capillaries (Fig. VIIIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). In hermaphrodites, the testis lies on the oral side of the lateral vessel and the ovary on the anal side. In dioecious species, gametes, as a rule, develop both in the left (around the left lateral vessel) and in the right (around the right lateral vessel) coelomic chambers (Fig. VIII (2)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
Phoronids have two types of sexual glands: nidamental glands and lophophoral organs. They are pair formations, situated in lophophoral concavity along the inner tentacles row, and are essentially overgrown epithelium. Lophophoral organs are developed in hermaphrodite species and the males of dioecious species (Fig. VIII (3)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Nidamental glands are present only in species, which is known by the care of generation, i.e. brood their eggs (to the stage of early larva) in lophophoral concavity. Eggs and embryos are agglutinated by nidamental glands secretion, forming embryonic congestions (one or two), which are well seen in the crown of tentacles (Fig. II (2)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
All phoronids are characterized by external-internal fertilization. Males discharge spermatozoids into surroundings, which in most species are formed into spermatophore, where the final maturation of male gametes occurs. Spermatophore gets (due to the high population density) into the female tentacular crown, and spermatozoids penetrate into the body coelomic cavity through metanephridia, where fertilization occurs. Phoronids spawn by fertilized eggs, and maturation divisions just may happen in the body cavity. Phoronids have radial cleavage, and blastula is the result of such process. Blastopore reduces towards the anterior part, and the remaining opening becomes a mouth. After that a larva is formed.
Most phoronid species have planktotrophic larvae – actinotrochs. Bottom lecithotrophic larvae are typical for the only one species – nanous burrowing phoronid Phoronis ovalis (see Silen, 1954). Plankton larvae of phoronids were originally described as separate organisms under the generic name “Actinotrocha” (see Mueller, 1846). Later A.O. Kovalevsky (1867) proved that actinotrochs were larvae of the bottom vermiform animals – phoronids, which were described earlier by Wright (1856). Since then phoronid larvae were repeatedly found in plankton of all regions of the World Ocean, and the number of the described larvae rapidly exceeded the number of the described adult forms. Thus, 20 larval species are known per 12 described adult phoronids (see, for example, Emig, 1982). The larvae of only two phoronid species - Phoronis ijimai (Actinotrocha vancouverensis) and Phoronopsis harmeri (A. harmeri) – were registered in the plankton of the Sea of Japan. Besides the larvae of these two species, in the Vostok Bay plankton we have found unknown before larvae, probably belonging to Phoronis hippocrepia species, and adduced them in the present work as Actinotrocha sp. The larvae ofPhoronis muelleri (A. branchiata), Ph. psammophila (A. sabatieri)and Ph. hippocrepia (A. hippocrepia) were not registered in the Sea of Japan. The larva of Ph. svetlanae was not described.
Actinotrochs of all phoronids are arranged according to a common structure. Their body consists of episphere (pre-oral blade), overhanging the mouth, hyposphere with a spindle of tentacles and terminal telotroch (Fig. IX (1)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Tentacles circle is open on the dorsal body part, where epi- and hyposphere join. The shortest tentacles are situated here, and the zone of new tentacle formation as well.
All actinotrochs have several ciliary cords, formed by long densely situated cilia: pre-oral (prototroch) running along the edge of the head blade, post-oral (metatroch) running along the tentacle spindle on abdominal and lateral body parts behind the mouth, and the terminal telotroch (Fig. IX (1)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). The latter is practically not expressed in early larvae. Conspicuous long cilia of parietal plume, which marks aboral organ (noticeable ectoderm thickening), apically situate on pre-oral blade (Fig. IX (1)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Protocoel, which borders are well visible in young actinotrochs and larvae lacking pigmentation, locates under the aboral organ (Fig. IXhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). The protocoel shape of larvae is an identification feature of a genus. Thus, the protocoel of Phoronopsis genus larvae has a shape of a cylinder (Fig.IXhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). On microscopic section coelomic cylinder is two septa, formed by mesodermal cells and limit the first coelom cavity by a narrow area under the apical plate (Fig. IXhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). In Phoronis genus larvae protocoel has only back wall and remains open at the front (Fig. Xhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">; XIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). All area from the back wall of protocoel to the edge of pre-oral blade is filled with mesenchymatous cell bars (Fig. X (2)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">; XIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
Only for adult larvae, ready for metamorphosis, species belonging can be identified reliably. Phoronid larvae sizes may be very considerable – up to 2.5 mm, but in some phoronid species small larvae occur, which size does not exceed 0.5-0.8 mm. Pigmentation, the number of tentacles, the amount of blood cell erythrocyte congestions are very important for the identification of phoronid larvae.
On the early developmental stages larvae have a transparent coverings, which allows to distinguish digestive tract departments (vestibulum, oesophagus, stomach, hind intestine), protonephridia, coelomic pavement (Fig. X (1)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). On the later larval stages ventral side of the upper stomach part (immediately under oesophagus) forms a diverticulum – a hepatic outgrowth, the walls of which are formed by thickened glandular, often pigmented epithelium (Fig. IXhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">, Xhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">, XIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Hepatic outgrowth can be unpaired (Fig. IX (2, 4)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">) or pared (Fig. XIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Larvae of some species at later developmental stages, as a rule, on the stage of 8 tentacles, have pigmented coverings. Location of pigment and its color depend on species. Pigment may locate in the ectoderm of oral field, along the edge of pre-oral lobe, on the ends of tentacles, in the basis of tentacle circle (Fig. Xhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">, XIIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">, XIIIhttp://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">). Sometimes pigment accumulations form well defined dark pigment spots – “eyes” – along the edge of pre-oral lobe (Fig. X (3, 4)http://biota/phoronida/plugins/system/jcemediabox/img/zoom-link.gif) 100% 50% no-repeat transparent;">).
A number of the tentacles of larvae increases with their age. Nevertheless, for every species there is a fixed maximal number of tentacles, which is amounted to by the premetamorphosis period. Maximal number of tentacles – 42 – is known for A. branchiata (Phoronis muellerilarva), minimal – 10 – for A. hippocrepia and A. pallida. In some larvae (A. sabatieri и A. branchiata) before metamorphosis rudiments of definitive tentacles appear, having a shape of small tubercles and locating under larval tentacles in their basis.
Erythrocyte congestions appear in mature larvae and have a shape of the big spherical formations of pink or scarlet (before metamorphosis) color, which can be seen through the covers of living larvae. Their maximal number is described for A. harmeri – 4: one pair occupies dorso-lateral position near young tentacles, and another one is situated ventro-laterally at both sides of the hepatic outgrowth. The number of erythrocytes congestions may be odd – 3 (A. sabatieri): one accumulation on each side of the hepatic excrescence and one accumulation is in the middle of the ventral side. Two ventral accumulations are described for A. branchiata(Selys- Longchamps, 1907) and for A. hippocrepia (Emig, 1982). One ventral accumulation of blood cells in the anterior stomach part is noticed for A. pallida.
A so-called frontal organ appears before metamorphosis in larvae of some species (Phoronis muelleri, Phoronopsis harmeri). The frontal organ of living larvae looks like an conspicuous thickening of the medial nerve of pre-oral lobe and act like chemo-receptor during metamorphosis (Emig, 1982).
A complete synonymy of phoronid species is given in the works of Christian Emig, a French zoologist (Emig, 1974, 1979).
This phylum includes one class Phoronida with a single order Phoronidea and family Phoronidae. The Sea of Japan and adjacent Okhotsk Sea area (Aniva Bay) is inhabited by 8 phoronid species, six of which are related to Phoronis genus (Ph. ovalis, Ph. psammophila, Ph. muelleri, Ph. ijimai, Ph. svetlanae, Ph. hippocrepia), and two species – to Phoronopsisgenus (Ph. harmeri and Ph. albomaculata).