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The World of Protozoa, Rotifera, Nematoda and Oligochaeta

Nolaclusilis

Nolaclusilis Snyder & Brownlee, 1991 (ref. ID; 4342 original paper)

Class Spirotrichea Butschli, 1889: Subclass Choreotrichia Small & Lynn, 1985: Order Choreotrichida Small & Lynn, 1985: Suborder Tintinnina Kofoid & Campbell, 1929: Family Tintinnidiidae Kent, 1881 (ref. ID; 4342)
Family Nolaclusiliidae (ref. ID; 7056 original paper)

[ref. ID; 4342]
Etymology; The genus name Nolaclusilis, or "easily closing little bell", refers to the morphology and function of the unique lorica of this organism. (ref. ID; 4342)

[ref. ID; 7056]
Snyder & Brownlee place Nolaclusilis bicornis within the family Titinnidiidae citing similar oral and somatic infraciliary patterns as key characters. A stomatogenesis which is initiated internally, low KDI values, and a lack of specialization of somatic cilia are traits found in the Tintinnidiidae (but in other tintinnines as well [Small, pers. observ.]) and these traits are found in both N. bicornis and N. hudsonicus. However, differences in the somatic kinetomes of species included within the Tintinnidiidae and Nolaclusilis species exist. A posterior kinety is present in N. hudsonicus, although apparently lacking in N. bicornis. This structure is described as being absent in the Tintinnidiidae. The presence of a anterior kinety, the curvature of the ventral kinety, and the absence of dorsal kinetal fragments or a dorsal kinety combine to create a kinetome pattern uniquely different from any other previously described tintinnine family. If lorica characters alone are considered diagnostic for inclusion within a family then both species with their single layered, hyaline diaphanous loricae would best fit into the family Tintinnidae. The lorica of Nolaclusilis spp., however, dose not conform to the other described genera and species found in this family. The ability of both Nolaclusilis species to bent or collapse their lorica, as well as the lateral appearance of the trophic cell, further distinguishes them from other tintinnines. The unique combination of kinetome, lorica, and behavioral characters warrant family level status for the genus. We propose that the family name, Nolaclusiliidae n. fam., be erected to include the genus Nolaclusilis and its two described species N. bicornis and N. hudsonicus n. sp. (ref. ID; 7056)
  1. Nolaclusilis bicornis Snyder & Brownlee, 1991 (ref. ID; 4342 original paper, 7056)
  2. Nolaclusilis hudsonicus Sniezek, Capriulo, Small & Russo, 1991 (ref. ID; 7056 original paper) reported author and year? (ref. ID; 4342)

Nolaclusilis bicornis Snyder & Brownlee, 1991 (ref. ID; 4342 original paper, 7056)

Descriptions

  • Lorica: Simple, hyaline, bell-shaped, lacking collar or agglomerations, short aboral spine may be present in some specimens. Flexible and collapsible, generally flattened in preserved specimens and in contracted live specimens. Dimensions of flattened loricae: mean length=37.3 um (range=24-46 um); mean width=37.6 um (range=22-47 um); n=115. (ref. ID; 4342)
  • Cell: Dimensions of Bouin's fluid-fixed cells: mean length=37.3 um (range=19-35 um); mean width=21.9 um (range=15-28 um); n=115. Bilaterally symmetrical with two prominent anterior horn structures as lateral extensions of the preoral ring. Fourteen oral polykinetids with cilia up to 15 um long. Position of the oral polykinetids variable with cell contraction. One polykinetid descends toward the cytostome, located internal to the right horn, and one polykinetid lies completely within the infundibulum adjacent to the descending polykinetid. Paraoral membrane along dorsal wall of the infundibulum. Internal stomatogenesis. Somatic kineties extend posteriorly on quarter to one half the cell length from just below the preoral ring, and range left and right from ventral to just part the horns with decreasing numbers of kinetids per kinety. Most of the dorsal surface barren. Anteriormost kinetids of all kineties, except the ventral, R2 and R3, consist of paired kinetosomes, all others monokinetids. Dikinetid cilia long, 5 um on the ventral surface to 20 um under horns. Monokinetid cilia shorter, 2-3 um. Generally two macronuclei and two micronuclei. (ref. ID; 4342)

    Remarks

    This tintinnine exhibits a strong bilateral symmetry of both the lorica and cell outline. In live cells, the lorica collapsed flat as the cell contracted into its base. Empty loricae that retained the smaller flattened shape as loricae containing contracted cells were also found in fixed samples. It is speculated that the collapse of the lorica is hydrodynamic in nature, caused by a jet of water displaced from within in the base of the lorica. The velocity of the expelled water would result in lower internal pressure relative to the water outside the lorica, thus causing the lorica walls to move inwards above the contracting cell. The axis of lorica collapse reflects the bilateral symmetry of the cell; the two horn structures are aligned with the inside corners of the flattened lorica. The small aboral spine on the lorica was first seen in scanning electron micrographs, and appears to be truncated or invisible in most specimens observed with light microscopy. The two prominent horns projecting laterally from opposite sides of the cell as extensions of the preoral ring are unique among described tintinnines. The preoral ring in other tintinnines (Laval 1972; Brownlee 1977) is composed of microtubules that descend from the oral membranelles. The composition of the "horn" material extending from the preoral ring in this specimens is unknown. The preoral ring appears to provide structural integrity to the oral region of the ciliate. Despite various distortions of cells due to contraction and fixation, the oral portion of the cell remained consistently circular. Each of the 14 (13-14) oral polykinetids is composed of two rows of kinetosomes and a patch of dark staining granules at the base of the two rows. These granules are probably associated with tentaculoids [Dr. E.B. Small, pers, commun.]. Twelve of the oral polykinetids are located on the outer surface of the expanded cell, with two located within the infundibulum progressively closer to the cytostome. The oral polykinetid closest to the cytostome and the posterior portion of the polykinetid immediately to the left lie within the infundibulum of the cell below the peristomial lip, even when the peristome is expanded. The position of the oral membranellear polykinetids varies with the contraction and expansion of the peristomial lip. In the contracted position, the peristomial lip and oral polykinetids are rotated inward so that the latter lie along the inside margin. When expanded, the peristomial lip rotates out so that the membranelles lie facing up. Despite this movement of the peristome, the oral polykinetids do not appear to curve with the peristomial lip, as in other tintinnids; rather, they appear to be structurally rigid, deforming the peristomial lip to conform to their position. The kinetosomes of the paroral membrane begin near the cytostome, course anteriorly and to the right along the dorsal interior wall of the oral cavity and end on the dorsal side of the infundibulm below the peristomial lip. Formation of daughter cell oral polykinetids (stomatogenesis) prior to cell division occurs internally. The kinetid map, shows the distribution of somatic kinetosomes on the cell surface and the oral polykinetids on the peristomial lip in relation to each other. The conventions of dorsal and ventral used here are those proposed by Brownlee (1977). The kineties extend under the horns but do not completely surround the cell, with a Kinetal Density Index (KDI) value of 0.14. The anteriormost kinetid of each kinety consists of paired kinetosomes except for the ventral kinety, R2, and R3, which are composed entirely of monokinetids. The ventral kinety begins at the level of the paired kinetosomes, anterior to R3. Unlike the other kineties of the cell, it extends initially perpendicular to the anterior-posterior axis of the cell parallel to the preoral ring. To the left of R2, the ventral kinety descends posteriorly. Kinetosomes of the anterior two-thirds of this kinety are closely spaced, making enumeration difficult (estimated to be 20-25 for the entire kinety). R2 and R3 are specialized kineties without anterior dikinetids. The range of kineties found to the right of the ventral kinety (including the ventral kinety) was 13-15 (n=10). The range of kineties found to the left of the ventral kinety was 16-18 (n=10). The elongate cilia of the paired kinetosome kinetids extend anteriorly to the rim of the lorica. These cilia are shortest between the horns on the ventral surface (5 um long), and longer in the region of each horn (to 20 um), extending out, but not attached to, each anterior corner of the lorica. The function of these elongate cilia is unknown. The somatic kineties do not extend entirely around the cell, leaving most of the dorsal surface barren of kinetosomes and cilia. Contraction of cells was always greater on the ciliated ventral surface, tilting the preoral ring and the entire anterior portion of the cell about the axis of the horns into the same plane as lorica collapse. Macronuclei were found to be highly variable in shape and size within a given population. The most common, but by no means dominant, configuration is two separate macronuclei with no discernable connection. Micronuclei are not always visible, but more than two were never observed. The lorica of Nolaclusilis bicornis n. g., n. sp. is identical in morphology and function to that described for N. hudsonicus n. sp. (Sniezek et al. 1991), with the exception of an aboral spine which was sometimes observed on specimens of N. bicornis. The variation in lorica size for N. bicornis encompasses the size range reported for N. hudsonicus (Sniezek et al. 1991). Cell morphologies of the two new species are similar, and although the cell size range reported of N. bicornis overlaps, it is slightly smaller than N. hudsonicus. Both specimens appear to have the horn structures that convey bilateral symmetry to this protist, although the interpretation of their function and connectedness to the loricae differ. The dorsal surface of both species is barren of kinetosomes. Slight differences in the somatic kinety distribution pattern the ventral surface are apparent, especially the presence of a posterior kinety in N. hudsonicus. N. bicornis n. g., n. sp. lacks the circumoral, prekinetal processes as described for N. hudsonicus. The number of oral polykinetids is two less for N. hudsonicus. The closest familial relationship appears to be the Tintinnidiidae, which previously consisted of two genera, Tintinnidium and Leprotintinnus. The family was originally created to include species thought to be primitive in nature, with very simple loricae, sometimes poorly defined or variable in shape, with or without agglutinated particles, and from marine, brackish, and occasionally fresh-water habitats (Corliss 1979; Marshall 1969). The loricae of the genus Tintinnidium, as defined by Marshall (1969), are "tube- or sac-formed or irregular, sometimes with a collar. Aboral end open or closed." The lorica of Leprotintinnus is defined (Marshall 1969) as "more or less cylindrical, open at aboral end. Sometimes a spiral structure present". The cytology of several species of Tintinnidium has been described based on protargol stained specimens (Foissner & Wilbert 1979; Laval-Peuto & Brownlee 1986; Brownlee 1977), although no such information exists for the genus Leprotintinnus. Available description characterize the family as having long kineties relative to cell length, the absence of posterior and dorsal kineties, little specialization of somatic cilia except K2 (=R2) and K3 (=R3), which may be set apart from and at an angle to the other somatic kineties, and a prostomial mouth. Stomatogenesis is internal, a feature unique for this family among all Tintinnina (Brownlee 1977, 1982). A low KDI value (0.2-0.3) is also considered to be characteristic of this group. The lorica of Nolaclusilis bicornis is different from Tintinnidium in the absence of agglomerated particles and from Leprotintinnus in its closed aboral end and ability to collapse. There are no reported cases of closing loricae for any other tininnine species, although one small Eutintinnus species (Family Tintinnidae) from the mesohyaline portions of the Bay has been observed to close its aboral opening (Brownlee, pers. observ.). The pattern of the somatic and oral infraciliature agrees well with those of the Tintinnidium species that have been described with protargol staining. Other than the peculiar position of the ventral kinety, and the slight skewness of R2 (= K2) and R3 (= K3), there is little differentiation of the somatic kineties and the lack of posterior and dorsal kineties is also consistent with the characterization of the family. The low KDI value (0.14) is more similar to that of the Tintinnidiidae (0.2-0.3) than to those of other families for which this index is known (0.44-0.54) (Brownlee, 1977). Contrasting features of N. bicornis to those of Tintinnidium include the relative shortness of the kineties to cell length and the absence of kineties over most the of the cell's dorsal surface. The absence of functional posterior and dorsal kineties in this family may be compensated for by the somatic kineties extending well posteriad. Cilia near the posterior part of the cell as posterior, dorsal, or elongated somatic kineties are thought to aid in water circulation within the lorica, particularly for the removal of waters. If indeed this is the case, N. bicornis may have obviated the need for such cilia by the flexible nature of the lorica, which would be fused on collapse. The extent of the barren region on the dorsal surface of the cell is also unique to N. bicornis, though a similar but smaller gap is found in Tintinnidium cylindrata (Foissner & Wilbert, 1979). We believe that this reduction is an adaptation associated with the asymmetrical contraction of the cell and the collapse of the lorica. The horns are also speculated to be adaptations involved in control of the unique lorica of this genus. In summary, the oral and somatic infraciliary patterns available from protargol silver stained specimens strongly suggest that Tintinnidium and Nolaclusilis bicornis belong to the same family, the Tintinnidiidae. Whether Leprotintinnus should remain in the family will depend on future cytological analysis of organisms in that group. The new genus, Nolaclusilis ("easily closing little bell"), is proposed on the basis of the unique morphology and function of the lorica, and the bilateral symmetry of the cell and lorica that separate N. bicornis from the other two genera presently in the family Tintinnidiidae. We do not feel that these differences necessitate the creation of a new family for the two species of the proposed genus as suggested by Sniezek et al. (1991). The importance of combining both cell and lorica characteristics in the taxonomy of the tintinnines is demonstrated by the present description. On the basis of lorica morphology alone, determination of the relatedness of N. bicornis to other tintinnines would have been a more difficult task than it has been with the additional, and perhaps more conservative (Davis 1978; Davis 1981; Laval-Peuto 1977; Laval-Peuto & Brownlee 1986; Brownlee 1977), information from the study of infraciliature. (ref. ID; 4342)

    Etymology

    The specific epithet bicornis refers to the two "horns" found on the cell of this type species for the genus. (ref. ID; 4342)

    Type locality

    Surface water of Back River Subestuary in the northern portion of the Chesapeake Bay estuary, Maryland, USA, 39 degrees 14.5'N, 76 degrees 23.0'W. (ref. ID; 4342)

    Type specimens

    A protargol-stained preparation of paratype specimens has been deposited as slide USNM 42453 in the ciliate type specimen slide collection, United States Museum of Natural History, Smithsonian Institution, Washington, D.C., USA. (ref. ID; 4342)

    Nolaclusilis hudsonicus Sniezek, Capriulo, Small & Russo, 1991 (ref. ID; 7056 original paper) reported author and year? (ref. ID; 4342)

    Diagnosis

    Small tintinnine. Lorica hyaline and chalice shaped with thele. Oral diameter 29.9-45.2 um. Lorica length 34.4-44.2 um. Troph length 25.0-36.9 um, width 23.3-31.7 um. Twelve OPKs as two rows, spiraled. "Capsules torquees" between OPKs. Two projections from peristome rim. Extrusomes in single circlet below OPKs, anterior to kinetal fragments. Twenty-two kinetal fragments, ciliated, dorsally absent. Posterior kinetal fragment. Pedicel attached to lorica side. Macronucleus bilobed. Two micronuclei. Zooid is contractile. Oligohaline waters. (ref. ID; 7056)

    Descriptions

  • Lorica: The chalice-shaped lorica is smooth, thin and hyaline and terminates in a minute, blunt thele. No collar, terminal spine, striations, or fenestrae are obvious. An average lorica length of 40.17+/-2.48 um (range=34.41-44.21 um) and width (oral diameter) of 40.23+/-3.37 um (range=29.90-45.21 um) was observed based on a measurement of 20 cells. (ref. ID; 7056)
  • Cell: Cell widths varied from 23.37-31.71 um (mean=28.02+/-2.16 um) and length from 25.01 to 36.96 um (mean=30.95+/-3.68 um) (n=20). Twelve equally spaced oral polykinetids (OPK) spiral around the peristome. Each OPK consists of two long kinetisomal rows of equal length. The cilia of both kinetosomal rows are of equal length. Irregularly sized, densely stained granules, perhaps comparable to the "capsules torquees" of Laval, appear to the immediate left and on the distal end of each OPK when viewed ventrally. No tentaculoid processes are visible. The peristomial rim is drawn out into single left- and single right-sided projections that appear to attach to the left and right margins of the lorica. We define left versus right with reference to the position of the ventral kinety. The terminal areas of these projections are somewhat flattened and are attached to the inside oral rim of the lorica. Internally these projections are tended by argentophilic fibers that reside immediately internal to the peristomial rim and link the projections to each other. The lateral projections give N. hudsonicus n. sp. bilaterality not present in other species. The position of the somatic kinetal fragments remains constant relative to these projections, so that the ventral surface contains kinetal fragments, and the dorsal surface contains a mid-dorsal space devoid of fragments. Single, well-stained processes of variable length lie anterior to the somatic kinetal fragments and are equally spaced around the perimeter, but below the edge of the peristomial rim. In noncontracted specimens, these processes extend over the oral edge of the lorica up to a distance one third or greater than the overall lorica length. These processes are thicker than stained somatic cilia and believed to be extrusomal. In specimens where the cell is contracted, the processes are shorter in length, but always longer than the somatic ciliature. With cell contraction, an inversion of the OPK region occurs and the peristomial region becomes elliptical. The somatic kinetid pattern consists of 22 kinetal fragments (KDI=0.25) consisting anteriorly of a dikinetid followed by successive monokinetids. The anterior kinetosome of the first paratene bears a longer cilium than that of the posterior kinetosome. The remaining somatic kinetosomes have shorter cilia of equal length. The kinety spacing relative to the oral ciliature is as indicated in Fig. 2. A posterior kinetal fragment consisting of 5-7 equally spaced monokinetids is found on the lower mid-ventral surface. A region of the dorsal surface (approximately 3 OPK lengths wide) is barren in any kinetosomal structures. No dorsal kinety was observed in any specimen. The cell is posteriorly attached to the lorica by a pedicel which adheres most often to the side of the lorica rather than the bottom. N. hudsonicus n. sp. possesses two micronuclei (about 2 um in diameter) adjacent to the single, bilobate macronucleus (11.4x5.1 um/lobe, n=20). Due to an extremely thin connection between the two lobes, the macronucleus may appear to be two separate macronuclei in some cells. All cells contained one to several vacuoles, most probably food vacuoles, each with a small, central, densely stained inclusion. (ref. ID; 7056)

    Notes

    Generic characters in common with the type species of the genus, N. bicornis Snyder & Brownlee, 1991 including the following: 1) the lorica is diaphanous, collapsible, of petite size and umbellate shape, 2) somatic kinetal fragments and a dorsal kinety are absent from the central part of the dorsal surface, and 3) bilateral symmetry is due to prominent lateral projections (referred to as "horns" by Snyder & Brownlee) from the peristomial rim of the zooid. This species differs from N. bicornis Snyder & Brownlee, 1991, the only other recognized species in the genus, in several respects. In contrast to the type species, in N. hudsonicus Sniezek, Capriulo, Small & Russo, 1991 1) the sizes of the troph and lorica are smaller, 2) the number of OPKs is fewer, 3) the number of kinetal fragments is greater, 4) no specialization of somatic kineties K2 or K3 is present, 5) a ventral kinetofragment below and to the left of the ventral kinety is present, 6) the lorica is not spinous, and 7) circumoral, prekinetal, extrusomal processes are present in this species and absent in the other species. Trichites have never been reported for tintinnine choreotriches. (ref. ID; 7056)
    N. hudsonicus n. sp. routinely collapses its lorica when living. The mode of lorica collapse for N. bicornis as described in Snyder & Brownlee differs from our description based on observation of the second species, N. hudsonicus. They suggest that the expulsion of water from within the lorica during cell contraction creates a lower internal pressure resulting in an inward collapse of the lorica. The axis of collapse in N. bicornis may be induced by the horn structures as the symmetry of the cell is reflected in the collapse. In N. hudsonicus, the axis of collapse occurs at 90 degrees to the long axis of the anterior cell perimeter. We suggest that the mode of collapse in N. hudsonicus involves both the projections from the peristomial rim and the pedicel. In the relaxed troph, the flattened tips of the peristomial projections extend to and adjoin with the lorica. When the pedicel contracts, the trophic cell is pulled posteriorly. Adherence of the projections to the lorica remains as the cell contracts. The result is a downward pulling effect exerted on the lorica at the two projection attachment sites. The lorica then buckles (collapses) at the weakest point midway between the attached projections. As a result, the plane lorica bending is dorsal-ventral across the oral opening of the lorica causing the posterior of the lorica to become bag-like and the anterior elliptical and wavy. (ref. ID; 7056)

    Type locality

    The ciliate was collected from the Hudson River near the Tappen Zee Bridge. Being a planktonic ciliate, physical parameters to the water probably determine where the species may be found. The ciliate was observed during the months of June, July, and August in low salinity (4-6.8 ppt) surface waters of the Hudson River. Surface water temperatures at time of collection ranged from 21.2-28.1 degrees C with corresponding oxygen measurements of 6.8-7.3 mg/L. Concurrent samples taken from deeper, higher salinity waters (10-20 ppt) failed to contain N. hudsonicus n. sp. (ref. ID; 7056)

    Type specimen

    The holotype remains in the collection of the senior author as part of a larger data set documenting the protist populations of the Hudson River estuary system. A Protargol stained preparation of paratype specimens will be deposited in the ciliate type slide collection, United State Museum of Natural History, Smithsonian Institution, Washington, DC, USA. (ref. ID; 7056)