Thigmokeronopsis rubra, Hu, 2004

Hu, Xiaozhong, 2004, Observations on the morphology and morphogenesis of a new marine hypotrich ciliate (Ciliophora, Hypotrichida) from China, Journal of Natural History 38, pp. 1059-1069 : 1060-1068

Thigmokeronopsis rubra sp. nov. (figures 1–35; tables 1, 2)

Type material

H  : one slide with protargol-impregnated specimens, collected from mollusc-culturing waters off the coast of Qingdao (Tsingtao), P . R. China (co-ordinates 36°08∞N, 120°43∞E), has been deposited in the Laboratory of Protozoology , Ocean University of China, Qingdao, P . R. China (ref. no. TPJ-96100201) .

P    : two slides with protargol-impregnated specimens (other details as for holotype) have been deposited as follows: one in the Laboratory of Protozoology , Ocean University of Qingdao, Qingdao, P . R. China (ref. no. TPJ-96100202) and one in the Department of Zoology , Natural History Museum, London, UK (reg. no. 2002:5:22:1) .

Etymology

The name is derived from the Latin word rubra (f.), meaning red, and alludes to the reddish appearance of this organism due to its numerous red cortical granules.

Diagnosis

Reddish marine Thigmokeronopsis , about 140–200 m m long in vivo. Two kinds of cortical granules: (1) pale yellow-green, distributed sparsely, (2) red, arranged in lines. Usually 7–11 left postoral ventral files. Two mid-ventral rows comprising a total of ca 51 cirri, extending almost to posterior end of cell. One buccal, seven transverse and two frontoterminal cirri. Bicorona with 11–16 frontal cirri. Thirty to 49 left and 28–45 right marginal cirri. Three complete dorsal kineties. membrane; FC, frontal cirri; LMR, left marginal row; Lv, postoral left ventral files; MVR, mid-ventral row; RMR, right marginal row; PM, paroral membrane; TC, transverse cirri. Scale bars= 40 m m. Description (figures 1–8, 22–24, 27; table 1)

Body 140–200 m m long in vivo, highly flexible and contractile, variable in shape but usually fusiform, left and right margins conspicuously convex, widest at midbody (figures 1, 6). Oral field about 25% body length with its proximal end slightly deepened in buccal cavity.

Pellicle flexible. Two kinds of sub-pellicular cortical granules, discernible only at ×1250 magnification: (1) pale yellow-green, about 1 m m in diameter, distributed sparsely and located peripherally; (2) medium or dark red, ca 0.5 m m in diameter, arranged in longitudinal lines, located deeper in cortex and giving body reddish appearance at lower magnification (figures 3, 24). Cytoplasm transparent, containing several food vacuoles. Numerous macronuclear nodules (>100, N =7), spherical to ellipsoid, about 3–7×1.5–3.5 m m, distributed throughout the body.

Cilia of adoral membranelles about 15 m m long, transverse cirri ca 18 m m long, other cirri 10–12 m m long.

Locomotion slow in comparison to some other hypotrichs (e.g. Parabirojimia similis ), crawling on substratum, occasionally stationary with thigmotactic cilia attached to substratum.

Infraciliature as shown in figures 4–8, 27. Adoral zone of membranelles composed of 33–43 membranelles, distal end curving to right ventral side; undulating membranes optically intersect each other in posterior region, paroral membrane ( PM) shorter than endoral membrane (EM) (figure 6); single buccal cirrus (BC) located near posterior portion of PM (figure 7). Bicorona comprising 11–16 frontal cirri ( FC) arranged in two rows, bases of cirri in anterior row enlarged. Two mid-ventral rows comprising a total of 40–59 (mean 51) cirri, extending almost to cell’s posterior. Six to eight transverse cirri ( TC) arranged in U-shape, occasionally two ventral cirri positioned anteriorly (figure 7, arrowheads). Seven to 11 inconspicuous, slightly irregular longitudinal rows of fine cirri forming left postoral ventral files (Lv), between left mid-ventral row and left marginal row. Thirty to 49 left and 28–45 right marginal cirri, marginal rows confluent posteriorly. Three complete dorsal kineties (figure 8, DK), dorsal cilia about 5 m m long. Caudal cirri absent.

1–3

Divisional morphogenesis (figures 9–21, 25, 26, 28–35)

Cortical morphogenesis in T. rubra occurs in two latitudinal developmental zones: an anterior field of the proter and a posterior field of the future opisthe. The first morphogenetic event within these zones is the initiation of oral primordia by a proliferation of basal bodies. In the proter, the oral primordium develops on the bottom and right walls of the buccal cavity while the paroral and endoral membranes are apparently still intact (figures 9, arrowhead; 25, arrow; 28, arrow). In the opisthe the oral primordium is formed as an anarchic field posterior to the adoral zone of membranelles, between the left ventral files and the left mid-ventral row (figures 9; 26, arrowhead). All mid-ventral cirri remain intact (ciliature and fibres present), indicating that parental basal bodies are not incorporated in the anlage. The oral primordia continue to grow by further proliferation.

Eventually, the opisthe’s anarchic field separates into anlagen for the adoral membranelles, undulating membranes (figures 10, arrowhead; 29, arrow and arrowhead) and fronto-ventral transverse cirri (FVT-cirri, figure 10, arrows). In the proter, one group of basal bodies appears to the right of the oral primordium; this is the FVT-anlage of the proter (figures 10, arrows; 26, arrows). The mid-ventral and the buccal cirri are still present, indicating that they are not involved in anlagen formation. This is strong evidence for a de novo origin of the adoral zone of membranelles ( AZM) anlagen, undulating membrane anlagen and FVT-anlagen.

In the next stage, the FVT-anlagen grow by increasing the number of basal bodies. Meanwhile, two anlagen originate de novo dorsal to each old marginal row (figures 11, 12, arrows). Likewise, the dorsal kinety anlagen form de novo: two anlagen are located near each old dorsal kinety (figure 12, arrowheads).

In intermediate dividers, new adoral membranelles begin to evolve in the opisthe, while in the proter the undulating membrane anlagen already appear to the right of the oral primordium and the old undulating membranes and buccal cirrus dedifferentiate (figure 13, arrowheads). Two FVT-anlagen organize into many oblique streaks posteriad (figure 13, arrows). Meanwhile the macronuclear nodules begin to merge (figure 30).

New adoral membranelles and undulating membranes continue to differentiate in a posteriad direction. A single cirrus develops from the anterior end of the undulating membranes anlage and later becomes the leftmost frontal cirrus (figures 14, 33). Subsequently the adoral zone evaginates.

Each FVT-anlage produces 27–34 oblique streaks of basal bodies (figures 30–32). Cirri develop from right to left, i.e. anterior frontal and right mid-ventral cirri first, then posterior frontal and left mid-ventral cirri, and left postoral and transverse cirri last. Both FVT-anlagen cross the parental mid-ventral rows but resorption of cirri was not observed in these regions (figures 14, 15). The marginal cirral anlagen gradually lengthen; however, the parental marginal rows are evidently fully intact at this stage. Several large macronuclear nodules are found clustered together and a few micronuclei begin to divide (figure 14, inset).

Later, the somatic ciliature is completely developed and the oral apparatus continues to develop. Starting from the posterior, the parental adoral membranelles are resorbed. The old left postoral ventral files are disintegrating and the parental buccal cirrus vanishes (figure 15). Simultaneously, a single branched macronucleus can be observed (figures 15, inset; 32, arrow).

The new buccal cirrus derives from anlage II (figures 34; 35, arrow). The frontoterminal cirri form as the rightmost cirri in the last FVT streak and subsequently move anteriad; the cirri to their left become transverse cirri. The other transverse cirri originate in the preceding four to seven streaks next to the mid-ventral cirri. All other cirri left of the new fronto-mid-ventral rows migrate posteriad and leftwards, forming the postoral ventral files.

In later dividers (figures 16–20), the anterior portions of the new adoral zones become distinctly curved. Marginal and dorsal rows are fully developed. Numerous ellipsoid macronuclear nodules are formed, some of which begin to divide. The parental adoral zone is almost completely resorbed. Disintegration is also evident within the old mid-vental, marginal and dorsal rows.

Reorganization in non-dividing cells resembles the development of the proter. It differs from the dividing form in that only one set of primordia is formed. Figure 21 show the infraciliature of the same individual in a late stage of reorganization.

Comparison with related taxa ( table 2)

Compared with Thigmokeronopsis jahodai Wicklow, 1981 , T. rubra has fewer adoral membranelles (38 versus ca 75) and dorsal kineties (three versus four), and has two types of cortical granules (yellow-green and red) versus only one kind (yellow-green) ( table 2).

Thigmokeronopsis rubra is distinguished from T. antarctica and T. crystallis mainly by having fewer adoral membranelles (38 versus 61–64), mid-ventral cirri (51 versus 93–97) and frontal cirri (11–16 versus 20–42), the possession of cortical granules (versus absent) and its biotope (marine water versus sea ice) (Petz, 1995).

Thigmokeronopsis rubra corresponds with its congeners with respect to the main morphogenetic events, i.e. in the origin and development of the opisthe’s primordia, the separate differentiation of the oral and somatic anlagen in the proter, the complete renewal of the parental AZM and the origin of the buccal cirrus. Additionally, the formation of marginal and dorsal anlagen is almost identical although Wicklow (1981) mentioned in his original descriptions that the anlagen develop within rows. However, his line diagrams and scanning electron micrographs show that they originate de novo, which is also indicated by apparently intact old marginal rows and by the occurrence of two anlagen near each parental structure, as described here for T. rubra . There are, however, some differences in Thigmokeronopsis jahodai , in particular the proter’s oral primordium is associated with the paroral membranes and buccal cirri whereas in T. rubra there was no such association. The mode of macronuclear division in T. rubra differs from that of its congeners. In T. antarctica and T. crystallis , for example, the macronuclear nodules fuse incompletely and several elongated macronuclei are found in the intermediate stages, whereas in T. rubra the macronuclear nodules fuse completely to form a single branched mass.

Certain features of the morphogenetic process also separate T. rubra from other urostylines. These include: (1) the formation of the marginal and dorsal anlagen which occurs de novo in T. rubra (versus within the parental structures); (2) the non-participation of the parental basal bodies in the formation of new ciliary structures (versus active participation); (3) the macronuclear nodules fuse into a single branched structure prior to division similar to that found in Metaurostylopsis marina (Kahl, 1932) Song, Petz and Warren, 2001 (versus a single round to elliptical mass) (Jerka-Dziadosz, 1972; Jerka-Dziadosz and Janus, 1972; Wirnsberger, 1987; Wiackowski, 1988; Mihailowitsch and Wilbert, 1990; Eigner and Foissner, 1992; Hu et al., 2000; Hu and Song, 2001a, 2001b; Song et al., 2001). It should also be noted that in Pseudokeronopsis , for example, every macronuclear nodule divides individually without prior fusion (Wirnsberger, 1987; Hu and Song, 2001a), and in T. antarctica and T. crystallis the macronuclear nodules fuse incompletely to form several segments before they separate again (Petz, 1995). Furthermore, anlage II is the origin of the buccal cirrus in both Pseudokeronopsis and Thigmokeronopsis . These peculiarities might indicate a closer relationship between Pseudokeronopsis and Thigmokeronopsis than had previously been supposed (Song et al., 2001).

As regards stomatogenesis, Thigmokeronopsis rubra resembles some morphologically related genera, i.e. Pseudokeronopsis , Pseudourostyla and Metaurostylopsis , in which the new AZM is formed from a separate primordium to completely replace the parental structure (Wirnsberger, 1987; Wiackowski, 1988; Hu and Song, 2001a; Song et al., 2001).