Eufolliculina
Eufolliculina Hadzi, 1951 (ref. ID; 7702)
Ciliophora: Family Folliculinidae (ref. ID; 7702)
[ref. ID; 7588]
General morphology and ultrastructural study. (ref. ID; 7588)
[ref. ID; 7702]
Diagnosis; Folliculinids producing loricae with a neck, without flaps or valves and with an unchambered ampulla. The lorica neck bears weak spiral sculptures or is unsculptured, it is shorter than the ampulla and opens slightly at the distal end as a brim. The lorica wall is single and not particularly thick. Lorica colour is yellowish, blue, blue-green or ruby red. The lorica attaches by a flattened basal part of the ampulla. Posterior end of ampulla is rounded or pointed. Lorica outline smooth. The two peristomial wings of the sessile cell may be rounded or pointed at their ends. The adoral zone of membranelles may form one to several spirals in the peristome before terminating at the cytostome. The sessile cell and swarmer have beaded macronuclei. The swarmer is produced as the anterior daughter cell during cell division. The swarmer is initially cylindrical, but this shape changes as the lorica is constructed. No contractile vacuoles at any stage. The sessil organism is typically blue, blue-green or green, is evenly ciliated and attaches to the lorica by a narrow foot. The genus contains two species, E. moebiusi and E. uhligi n. sp. (ref. ID; 7702)
Type species; Eufolliculina moebiusi (ref. ID; 7702)
- Eufolliculina ampullacea Hadzi, 1951 (ref. ID; 7702)
- Eufolliculina boltoni (ref. ID; 7588)
- Eufolliculina latemarginata (Hadzi) Hadzi, 1951 (ref. ID; 7702)
- Eufolliculina lignicola (Faure-Fremiet) Hadzi, 1951 (ref. ID; 7702)
- Eufolliculina moebiusi (Kahl, 1932) Hadzi, 1951 (ref. ID; 7702)
Syn; Eufolliculina ampullacea (Hadzi, 1938) Hadzi, 1951 (ref. ID; 7702); Eufolliculina latemarginata (Hadzi, 1938) Hadzi, 1951 (ref. ID; 7702); Eufolliculina mobiusi (Hadzi, 1938) Hadzi, 1951 (ref. ID; 7702); Folliculina ampulla pro parte of Mobius (1887) (ref. ID; 7702); Folliculina ampulla pro parte of Laackmann (1910) (ref. ID; 7702); Folliculina ampulla pro parte of Sahrhage (1916) (ref. ID; 7702); Folliculina ampullacea Hadzi, 1938 (ref. ID; 7702); Folliculina latemarginata Hadzi, 1938 (ref. ID; 7702); Folliculina moebiusi Kahl, 1932 (ref. ID; 7702); Folliculina mobiusi Hadzi, 1938 (ref. ID; 7702); Folliculinosis gunneri sensu (Faure-Fremiet, 1936) (ref. ID; 7702)
- Eufolliculina uhligi Mulisch & Patterson, 1983 (ref. ID; 7702 original paper, 7731) reported author and year? (ref. ID; 191)
Remarks
E. ampullacea Hadzi, 1951, was originally described by Laackmann (1910: Fig.10: Plate XIII) under the name Folliculina ampulla. Laackmann included many different organisms under that name, so his general comments about that species are not useful. His drawing shows a single contracted (fixed) cell in a lorica which ia attached to the substrate by its rounded ventral side and which has a pointed posterior end. The neck rises vertically, and has no collar. In view of the studies carried out on folliculinid lorica construction (Andrews 1920, 1923; Mulisch and Hausmann 1983; Uhling 1963, 1964) it seems likely that this description of attachment is inaccurate. This organism can then only be distinguished by having a posteriorly pointed lorica. Such a feature is included in the description by Mobius (Mobius 1887) of the organism eventually to be called E. moebiusi. Although Hadzi (Hadzi 1951) elevated the organism described by Laackmann (1910) to the status of specis, we regarded it as being identical to E. moebiusi. (ref. ID; 7702)
Remarks
E. latemarginata (Hadzi) Hadzi, 1951, was first illustrated by Sahrhage (1917: Fig.1(33): Pl.10) as Folliculina ampulla, once again with organisms belonging to other species. He comments that his drawing is schematised. As Sahrhage did not distinguish between organisms which we now recognize as different species, his general comments are ambiguous. Hadzi (1938) distinguished the organism as the species F. latemarginata, transferring it to the genus Eufolliculina in 1951. Faure-Fremiet (1936) described a folliculinid under the erroneous name of Folliculinopsis gunneri, believing it to be what is now called Pachyfolliculina gunneri (Dons) Hadzi, 1951. Hadzi regarded the organism described by Faure-Fremiet as identical with E. latemarginata. Both organisms have relatively pointed wings, although the wings are broader in Sahrhage's description than in Faure-Fremiet's. The latter author indicatd a ruffled lorica-neck and a less prominent rim than did Sahrhage. Hadzi's synonymy is therefore in doubt, but we can accept it because of the uncertainty over Sahrhage's description. We rely then on Faure-Fremiet's description for most diagnostic features. Under these conditions, E. latemarginata sensu Hadzi resembles E. moebiusi sensu Hadzi. Both organisms are of comparable sizes, both have relatively pointed peristomial wings, both have a yellowish lorica divided into an ampulla with a rounded end and opening as a slight brim. Macronuclear characters are also comparable, although the organisms differ in their habitat. Faure-Fremiet refers to his organism as being deep dark blue, whereas that of Mobius, according to Hadzi, is dark green. As Mobius' statement is uncertain, and in view of overall similarities of these two populations, we recognize both as E. moebiusi. (ref. ID; 7702)
Remarks
E. lignicola (Faure-Fremiet) Hadzi, 1951 was described by Faure-Fremiet (1936) as Folliculinopsis lignicola for a single organism within a hollow tube in wood. The lorica has no neck and is thus unlike other members of the genus Eufolliculina. It is also distinguished from Stentofolliculina, also without a neck, by not being attached by the base of the lorica. Hadzi's placement of this organism is therefore uncertain. (ref. ID; 7702)
Synonym
Eufolliculina ampullacea (Hadzi, 1938) Hadzi, 1951 (ref. ID; 7702); Eufolliculina latemarginata (Hadzi, 1938) Hadzi, 1951 (ref. ID; 7702); Eufolliculina mobiusi (Hadzi, 1938) Hadzi, 1951 (ref. ID; 7702); Folliculina ampulla pro parte of Mobius (1887) (ref. ID; 7702); Folliculina ampulla pro parte of Laackmann (1910) (ref. ID; 7702); Folliculina ampulla pro parte of Sahrhage (1916) (ref. ID; 7702); Folliculina ampullacea Hadzi, 1938 (ref. ID; 7702); Folliculina latemarginata Hadzi, 1938 (ref. ID; 7702); Folliculina moebiusi Kahl, 1932 (ref. ID; 7702); Folliculina mobiusi Hadzi, 1938 (ref. ID; 7702); Folliculinosis gunneri sensu (Faure-Fremiet, 1936) (ref. ID; 7702)
Diagnosis
Eufolliculina with yellow or yellowish lorica having a pointed or rounded posterior end. Neck rises at 30 degrees to 90 degrees from substrate, with little sculpturing and conical widening of the neck but lacking a distinct brim. Cell dark green or dark blue. Lorica 200-250 um long when viewed from above, extended cell approximately double that. Macronucleus with 8-14 beads. Adoral zone of membranelles completing more than two turns in peristome. Wings equal in length, not noticeably broad and with pointed tip. (ref. ID; 7702)
Remarks
E. moebiusi (Kahl, 1932) Hadzi, 1951, was described by Mobius (1887: Figs.1-4, 8-21) as Folliculina ampulla. Mobius described other organisms, subsequently designated as different species, under that name. Consequently and general comments in the next are deemed ambiguous. Kahl (1932) distinguished F. moebiusi as a separate species and it was placed in the genus Eufolliculina by Hadzi (1951) under the name E. mobiusi. The original description is confused. The size in the text does not agree with that in the figure, a point not detected by Kahl. Mobius' original drawing shows a double spiral in the peristome, almost certainly an error, and the text indicates that the lorica may adopt a range of colours. In veiw of this ambiguity, we adopt the interpretation of Hadzi (1951) as to the diagnostic features of this organism. (ref. ID; 7702)
Eufolliculina uhligi Mulisch & Patterson, 1983 (ref. ID; 7702 original paper, 7731) reported author and year? (ref. ID; 191)
Diagnosis
Eufolliculina with blue-green (occasionally ruby-red) lorica, always with rounded posterior end. Neck rises about 45 degrees from substrate, is shorter than the ampulla and expands slightly into a brim. The neck is sculptured weakly by a spiral making 3-4 turns. The lorica is about 300 um long. The cell has a light deep green-blue colour. Macronucleus with about 14 beads. The adoral zone of membranelles makes one and a half turns before terminating. The relatively narrow peristomial wings may have rounded or pointed tips. (ref. ID; 7702)
Descriptions
The sessile cell inhabits a blue-green lorica. When first formed the lorica is translucent, but as ages it becomes more opaque. Under cultural conditions it can take a ruby-red colour. At the light-microscopal level the single layered lorica wall appears slightly uneven. The lorica is attached to the substrate by a basal plate which is hardly visible by light-microscopy but can be detected easily by scanning electron-microscopy. Part of the lorica is expanded to form the ampulla into which the organism withdraws when it contracts. The ampulla extends away from the substrate as a cylindrical neck. The neck is weakly sculptured by a spiral curvature making about 4 turns. Typically, one sessile organism inhabits each lorica. It is attached to the posterior rounded pole of the ampulla by a holdfast. The holdfast is a thin drawn out extension of the posterior of the cell, appearing slightly expanded and hyaline where it makes contact with the lorica. The sessile organism has the same blue-green colour as the lorica, but becomes darker and more opaque before division. Two wings protrude from the aperture of the lorica in feeding, uncontracted cells. The adoral zone of membranelles passes first around the edge of the right wing, then the left wing (as seen from the dorsal view) before entering the peristome. It makes about 1.5 turns within the peristome before terminating. The slightly curved wings are similar in length and may or may not have pointed tips. The right wing widens slightly at its base. The cytproct is located just below the base of the left wing. The somatic cilia occur in about 60-65 kineties, an estimate obtained from scanning electron micrographs of two cells. The macronucleus takes the form of a string of nodes. There are several micronuclei alongside the macronucleus but these are difficult to see. These is no contractile vacuole complex visible. The appearance of the sessile organism depends on a number of factors. The size and optical density are affected by the recent feeding history of the organism. A fully gorged organism may have difficulty in retraction into the lorica, and the wings may appear broader and shorter than usual. Occasionally one encounters cells within clones that are unusually small (350-400 um) and lightly coloured. Under cultural conditions, sometimes more than one sessile organism is found within the same lorica; occasionally cells may have extra peristomial wings. Swarmer production typically follows extensive feeding. It is first indicated by the resorption of the peristomial wings, by an accumulation of pigment at the anterior end of the cell and by the condensation of the macronucleus. In some cases these events do not continue as swarmer production, but simply lead to the formation of re-organized feeding structures. When the cell divides, two new membranellar anlagen form. The anterior one produces the membranelles of the swarmer (Uhlig 1973). After 4 or so hours, the swarmer separates from the front of the parent cell as a dark coloured cylindrical organism. It has a small anterior spiral of membranelles but is unable to feed. At the time of separation is has a beaded macronucleus. After a certain free-swimming phase (Uhlig 1978), the swarmer starts to explore the substrate and eventually selects a site for settling. It then produces a lorica, changing its shape as lorica construction proceeds. When completed, the anterior membranelles are resorbed and the feeding structures of the sessile stage develop. The process of lorica construction takes about 4 hous depending on the temperature of the medium. The number and size of the macronuclear nodes, and the number of kineties in the swarmer are similar those of the sessile form. (ref. ID; 7702)
The Oral Apparatus:
- Adoral membranelles. The adoral zone of membranelles (AZM) begins at the base of the right peristomial wing and extends around the margin of both wings. At the base of the left wing in enters the buccal cavity where it completes about one and a half turns. At the peristome each membranelle consists of two longer and one short row of cilia. The first and most posterior row contains 14 cilia, the second row 12, and the third row 3 cilia. The kinetosomes of the posterior row can be recognized by the presence of postciliary microtubules. Using this marker, one can see that the rightmost kinetosome of the posterior row is displaced anteriorly, so it lies in line with kinetosomes of the second row. Parasomal sacs occur posterior and to the right of the membranellar kinetosomes. Membranous cisterae may be common in the vicinity of membranelles. Several microtubular systems arise from kinetosomes of the membranelles. The kinetosomes of the most posterior row of each membranelle give rise to a postciliary ribbon of about 8 microtubules. This ribbon terminates in the septae which separate adjacent membranelles. Transverse microtubules arise only from the most anterior kinetosomes of each membranelle. They are difficult to see as they arise in electorn-dense material. They are composed of 2-5 microtubules which rise rapidly into the septae. From the bases of the kinetosomes of the longer rows of cilia arise nemadesmal microtubules. These initially are arranged in ribbons. However, as they pass into the cytoplasm they form bundles, joining up with nemadesmal microtubules of adjacent rows. The bundles then turn about 90 degrees and pass in the direction of the paroral kinety at the peristomial field. Viewed in cross-section, the nemadesmal microtubules may be seen to be hexagonally packed in three rows, with individual microtubules connected together by links. Near the paroral kinety, the nemadesmal fibres of adjacent membranelles join together and terminate here. The kinetosomes within each membranelle are interconnected by an elaborated network of electron-dense filaments. One set of fibres is particularly well developed. These are the fibres which connected triplet no. 3 of the kinetosomes of the second row with triplet no. 2 of kinetosomes in the most anterior row. The orientation of the membranelles and the distance between them depends on the degree of extension of the peristomial wings. The inclination of the kinetosomes also varies with the degree of wing extension, being inclined towards the anterior in extended cells and lying more uprignt in contracted cells. By passing the tip of the wing, the AZM inverts its direction regarding the anterior-posterior axis of the cell. However, the construction of each membranelle remains the same, i.e., the sequence of the individual rows and the arrangement of the kinetosomal rootlet structures. On the ventral side of the left wing and on the dorsal side of the right wing, the postciliary microtubules extend towards the anterior end of the cell. The AZM is flanked by two bundles of myonemes which run parallel to it along the peristomial wings. There are also small myonemal strings which underlay the bases of the membranellar kinetosomes and interconnect the AMs (Mulisch et al. 1981). The AZM broadens at the base of the left peristomial wing, just before entering the buccal cavity. In this region the paroral kinety terminates. In the first turn of the AZM, the number of cilia of each membranellar row increases to 30 or 36, with the third row enlarging to be made up of as many as 26 cilia. It is hard to be precise about the total number of cilia as the rows are curved and pass out of the plane of section. In this same region the distance between the membranelles increases. The AZM then curves towards the dorsal side of the body and enters the buccal cavity. The membranelles in the buccal cavity have a similar organization to those of the peristomial region. The transverse microtubules rise less sharply and are made up of 7 microtubules. These include one row of 5 or 6 microtubules, and one or two additional ones which lie in front of the row and more adjacent to the kinetosomes. Filamentous connections among kinetosomes appear to be more strongly developed in the buccal area. There is no specific association between membranelles and myonemal structures as is found in the wings. However, a large bundle of myonemes follows the course of the AZM and surrounds the buccal cavity, internal to the nemadesmata. Deeper in the buccal cavity, the AZM makes a further turn to encircle the cytopharyngeal region. Here the number of cilia in each row declines of 25 to 30 with the third row disappearing finally. The process of reduction continues to the end of the AZM, with the membranelles becoming more tightly packed together and the septae disappearing entirely. The postciliary microtubules of the rightmost membranellar kinetosomes in this region are extremely elongated and extend deep into the cytoplasm, passing in the region of the nascent food vacuole. These are the "cytopharyngeal microtubules" and are broad ribbons of up to 30 microtubules. More distantly the arrangement of these microtubules becomes less organized. Between the cytopharyngeal ribbons one can find numerous flattened vesicles and cisternae. There is also a myonemal cord which surrounds the region of the nascent food vacuole. (ref. ID; 7731)
- Paroral kinety. The paroral kinety begins, like the AZM, at the base of the right wing, and runs parallel to the AZM. The kinetosomes are arranged in dyads. The anterior kinetosome of each dyad is ciliated. A single microtubule is associated with its microtubular triplet no. 4, and a ribbon of 5 postciliary microtubules is associated with the barren kinetosome. This also supports two transverse microtubules which are embedded in electron-dense material located between the kinetosomes. The lower part of the ciliated kinetosome is surrounded by an elctron-dense sheet which gives rise to bundles of microtubules. These "paroral microtubules" run perpendicular to the nemadesmata and terminate at them in electron-dense material. Near the first few kinetosomes of the paroral kinety, there are large microtubular bundles. These pass between nemadesmata of the right peristomial wing, and towards the buccal opening. They broaden at their ends to run just under the plasmalemma into the buccal cavity. (ref. ID; 7731)
Etymology
This new species is called Eufolliculina uhligi in honour of Dr. G. Uhlig, Biologische Anstalt Helgoland, BRD, who first isolated and culutred this organism. (ref. ID; 7702)
Type materials
E. uhligi n. sp. was isolated by G. Uhlig from rocky intertidal coasts of Helgoland, 18 years ago, and described briefly in Uhlig, 1965 (Uhlig, pers. comm.). Type material has been deposited at the British Museum (Natural History), London (Reg. nos 1982:11:10:1-2). (ref. ID; 7702)