Parallelostrombidium paralatum, Xu & Song & Warren, 2006

Xu, Dapeng, Song, Weibo & Warren, Alan, 2006, Morphology and infraciliature of two new species of marine oligotrich ciliates (Ciliophora: Oligotrichida) from China, Journal of Natural History 40 (21 - 22), pp. 1287-1299 : 1288-1294

Parallelostrombidium paralatum nov. sp.

( Figures 1 , 2 ; Table I)

Diagnosis

Marine Parallelostrombidium , in vivo about 70× 60 mm; dorsoventrally flattened ca 2:3; cell ellipsoidal in outline with conspicuous apical protrusion; on average 27 anterior and 17 ventral membranelles; two posteriorly directed thigmotactic membranelles; macronucleus broadly ellipsoidal; extrusomes ca 10 mm long, arranged along equatorial area; girdle and ventral kineties with 71–99 and 32–42 dikinetids, respectively.

Etymology

The specific epithet refers to the superficial similarity in body shape between this species and Strombidium latum .

Type location

Shrimp-culturing waters in Jiaozhou Bay off Qingdao (Tsingtao, 36 ° 08 9 N, 120 ° 43 9 E), China .

Slide deposition

One holotype slide (registration number 2005:8:24:1) of protargol-impregnated specimens is deposited in the collection of the Natural History Museum, London, UK and two paratypes are deposited in the Laboratory of Protozoology , Ocean University of China (registration numbers 04:04:21:01 and 04:04:21:02) .

Description

Size in vivo 55–80× 50–65 mm, usually 70× 60 mm. Cell ellipsoidal in shape with bluntly rounded posterior end; when viewed from ventral side, usually broadest in the equatorial area ( Figures 1A , 2A ). Slightly flattened dorsoventrally ca 2:3 ( Figures 1B , 2D ). Collar region domed to form a conspicuous apical protrusion, 6 mm high ( Figure 2A , arrow), which may disappear or be undetectable after protargol impregnation. Buccal cavity relatively deep, extending obliquely towards right side of cell and terminating about onethird of the way down the cell ( Figures 1A , 2A ).

Cell extremely fragile, highly sensitive to presence of cover-slip and easily bursts. Pellicle delicate with thin and transparent hemitheca that covers posterior half of cell ( Figure 1A ), but no polygonal cortical platelets recognizable either in vivo or in silvered specimens. Cytoplasm colourless to greyish, containing many ingested algae (including diatoms) which often render cells opaque or dark when observed at lower magnifications ( Figure 2A ). Extrusomes prominent and acicular-shaped, ca 10 mm long, evenly arranged in a single row at about the level of the hemitheca margin, but not in bundles ( Figures 1A , 2E ). Neither contractile vacuole nor cytopyge were detected. Single macronucleus broadly ellipsoidal in shape and centrally located, containing several large nucleoli each, 5 mm across ( Figures 1I , 2H ); no micronucleus detected.

Locomotion with two patterns: moderately fast and irregular when swimming ( Figure 1E ), or very fast when crawling on debris, using its two thigmotactic membranelles for attachment with ventral side facing down ( Figure 1F ).

Somatic ciliature as shown in Figures 1 and 2 , consisting of one girdle kinety and one ventral kinety. Girdle kinety originates in mid-ventral region (to the left of the ventral kinety) and extends transversely across right ventral and dorsal sides, curves obliquely across left ventral side of cell and terminates at mid-caudal area ( Figures 1C, H, I , 2G, I ). On average there are 84 (71–99) widely spaced dikinetids. Within each dikinetid, the left basal body bears a short cilium about 2 mm long while the right is subtended by a conspicuous argentophilic fibre ( Figure 2G, I , arrows). Ventral kinety, which is composed of about 38 (32–42) densely arranged dikinetids, extends anteriad from posterior pole, parallel to the distal end of the girdle kinety and terminates at equatorial level ( Figures 1C, H, I , 2I , double-arrowheads). Each dikinetid has a cilium (about 2 mm in length) associated with the anterior basal body. Girdle kinety and ventral kinety thus both with same orientation. No extra kinety detected.

Oral apparatus occupies anterior end of cell, consisting of a short endoral membrane on inner wall of buccal lip and a membranellar zone ( Figures 1H, I , 2I ). Adoral zone of membranelles bipartite with an anterior portion of about 28 (26–30) membranelles and a ventral portion of about 17 (15–19) membranelles, all of which are composed of three kinety rows ( Figure 1D ). Cilia of most anterior membranelles ca 20 mm in length, stretching anteriorly when swimming ( Figure 1A ). Bases of anterior membranelles about 11–12 mm long. Anterior membranelles distinctly separated from ventral ones by the two thigmotactic membranelles, the bases of which are about 15 mm long ( Figures 1H , 2I , arrowheads). Cilia of two thigmotactic membranelles about 30–35 mm long and always directed posteriorly like two tails ( Figure 1A, B , arrowheads). Bases of ventral membranelles about 7–8 mm in length, distinctly shorter than those of the thigmotactic membranelles. Endoral membrane extending to centre of protrusion, probably composed of monokinetids ( Figure 1H ). Pharyngeal fibres not detected.

Stomatogenesis

Several stages in division were found which permit the reconstruction of the main stomatogenetic processes. Stomatogenesis commences with the apokinetal development of cuneate, longitudinally orientated basal bodies in a shallow depression underneath the ventral membranelles and to the left of the anterior end of the girdle kinety ( Figure 2C , arrows; J, arrowhead). While the oral primordium elongates posteriorly, membranelles differentiate from anterior to posterior ( Figure 2F , arrowhead) and the endoral membrane originates de novo. At the same time, new basal bodies are generated by intrakinetal proliferation ( Figure 1J , arrows). Simultaneously, the membranelles become ciliated. When the final number of membranelles is formed, the oral primordium moves to the left ventral side of cell. The oral primordium positions to the left of the anterior end of the girdle and ventral kinety and above the left portion of the girdle kinety ( Figure 1J ).

Comparison with related species

To date, approximately 12 species of oligotrich ciliates with thigmotactic membranelles inhabiting marine biotopes have been reported: Omegastrombidium elegans (Florentin, 1901) Agatha, 2004 ; Spirostrombidium urceolare (Stein, 1867) Lei et al., 1999 ; Spirostrombidium cinctum ( Kahl, 1932) Petz et al., 1995 ; Strombidium paracalkinsi ( Lei et al., 1999) Agatha, 2004 ; Strombidium calkinsi Fauré-Fremiet, 1932 ; Strombidium clavellinae von Buddenbrock, 1922 ; Strombidium sauerbreyae sensu Fauré-Fremiet, 1950 ; Strombidium fourneleti Dragesco, 1960 , Strombidium faurei Dragesco, 1960 , Strombidium latum sensu Kahl, 1932 , Strombidium latum sensu Fauré-Fremiet, 1950 , and Parallelostrombidium paralatum ( von Buddenbrock 1922; Fauré-Fremiet 1932, 1950; Kahl 1932; Dragesco 1960; Lei et al. 1999; Song et al. 2000; Xu and Song 2006; present study). The infraciliature of each of the first four species listed have recently been revealed ( Lei et al. 1999; Song et al. 2000; Xu and Song 2006). Based on those data they belong to genera other than Parallelostrombidium and so can easily be distinguished from P. paralatum . Although the infraciliature of Strombidium calkinsi Fauré- Fremiet, 1932 still remains unknown, it can easily be separated from P. paralatum by the position of the thigmotactic membranelles (dorsal versus ventral).

Fauré-Fremiet (1950) described two forms under the name Strombidium sauerbreyae , despite the fact that their morphology is quite different from that of the original ( Sauerbrey 1928). Considering the general morphology (namely cell size and shape, presence of the two thigmotactic membranelles, locomotion pattern etc.), S. sauerbreyae sensu Fauré-Fremiet, 1950 bears a strong resemblance to Parallelostrombidium paralatum , but it can be differentiated from the latter by (1) arrangement of extrusomes (sparsely arranged in the ventral side versus evenly arranged at about the level of hemitheca margin), and (2) much lower number of anterior membranelles (ca 17 versus 26–30) and ventral membranelles (ca 15 versus 15–19) ( Fauré-Fremiet 1950).

Strombidium latum sensu Fauré-Fremiet, 1950 also has thigmotactic membranelles. However, it can be separated from Parallelostrombidium paralatum by its much larger cell size (110–170 mm versus 55–80 mm), different distribution of extrusomes (surrounding the cell versus arranging along the equatorial area) and much larger oral cavity (about twothirds of cell length versus about one-third of cell length) ( Fauré-Fremiet 1950).

Strombidium latum sensu Kahl, 1932 has two to three thigmotactic membranelles, which should also be compared with Parallelostrombidium paralatum . The former can be separated from the latter by its much larger cell size (100–140 mm versus 55–80 mm), and different arrangement of extrusomes (surrounding the cell margin versus arranging along the equatorial area) ( Kahl 1932).

Strombidium fourneleti Dragesco, 1960 is similar in size to Parallelostrombidium paralatum and also has two thigmotactic membranelles. However, it can be distinguished from the latter by the cell shape (globular versus ellipsoidal), the fine adoral membranelles (versus prominent and well-developed), the presence of polygonal cortical platelets (versus absent), the sparsely distributed extrusomes (versus densely arranged), and the total number of anterior and ventral membranelles (, 24 versus 41–49) ( Dragesco 1960).

Strombidium clavellinae von Buddenbrock, 1922 is also very similar to Parallelostrombidium paralatum in terms of its general appearance ( von Buddenbrock 1922). It differs from the latter, however, in having four thigmotactic membranelles (versus two), and fewer membranelles (total of anterior and ventral membranelles 32–35 versus 41–49).

Considering the size and presence of two thigmotactic membranelles, Strombidium faurei Dragesco, 1960 should also be compared with Parallelostrombidium paralatum . The former differs from the latter in terms of cell shape (ovoid versus ellipsoidal and dorsoventrally flattened), total number of anterior and ventral membranelles (, 27 versus 41–49) and the arrangement of extrusomes (sparsely distributed on the somatic area versus densely arranged along the equatorial area) ( Dragesco 1960).

Ontogenetic comparison

Only early dividers were found in Parallelostrombidium paralatum , so comparisons between Parallelostrombidium and its congeners were based on stomatogenesis information.

The position of the oral primordium of Parallelostrombidium is very similar to that of Novistrombidium , i.e. oral primordium originates above the left portion of the girdle kinety ( Agatha 2003a).

Parallelostrombidium differs from Strombidium in the location of the oral primordium (anterior versus posterior portion of the girdle kinety) ( Song and Wang 1996; Agatha 2003a).

Similar to Laboea and Spirotontonia , the parental oral ciliature of Parallelostrombidium does not reveal any signs of reorganization. However, the position of the oral primordium of the latter is different from that of the former (oral primordium originates anterior to the left ventral portion of the girdle kinety versus oral primordium develops posterior to the left portion of the girdle kinety) ( Agatha et al. 2004).

Figures

Figure 1. Parallelostrombidium paralatum nov. sp. from life (A, B, E–G) and after protargol impregnation (C, D, H– J). (A) Ventral view of a typical individual; (B) lateral view, arrowheads show the two thigmotactic membranelles; (C) pattern of somatic ciliature; (D) details of the anterior membranelles; (E) pattern of locomotion; (F) to show the creeping state, note the cell attached to the substrate with its two thigmotactic membranelles; (G) extrusomes; (H, I) ventral (H) and dorsal (I) views showing ciliary pattern; (J) ventral view of a middle divider, to show the newly built oral primordium and new thigmotactic membranelles (arrowheads); basal bodies proliferate within the girdle and ventral kinety (arrows). AM, anterior membranelles; AP, apical protrusion; E, endoral membrane; GK, girdle kinety; Ma, macronucleus; Pe, pellicle; TM, thigmotactic membranelles; VK, ventral kinety; VM, ventral membranelles. Scale bars: 30 mm (A, B, H, I); 5 mm (G); 40 mm (J).

Figure 2. Photomicrographs of Parallelostrombidium paralatum nov. sp. from life (A–E) and after protargol impregnation (F–J). (A) Ventral view of a representative specimen, arrow marks the apical protrusion; (B) ventral view of the anterior region of the cell, to show the apical protrusion and the ventral membranelles; (C) ventral view of the posterior region of the cell, arrows mark the oral primordium of the opisthe; (D) lateral view, to show the apical protrusion and the ingested algae; (E) extrusomes after cell bursts; (F) early divider in left ventral view, arrowheads indicate the oral primordium; (G) dorsal view, arrows mark the girdle kinety; (H) to show the macronucleus and the nucleoli; (I) ventral view, to show the two thigmotactic membranelles (arrowheads), girdle kinety (arrows) and the ventral kinety (double-arrowheads); (J) early divider in left ventral view, arrowhead marks the oral primordium. Scale bars: 35 mm (A, D); 5 mm (E).