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The World of Protozoa, Rotifera, Nematoda and Oligochaeta

Ellobiophrya

Ellobiophrya Chatton & Lwoff, 1923(ref. ID; 1555, 3969, 7412)

Ciliophora: Peritrichia: Family Ellobiophryidae (ref. ID; 7412)

Synonym Claustophrya Naidenova & Zaika, 1969 (ref. ID; 3969)

[ref. ID; 3969]
Diagnosis; Cinctum with limbs joined to one another at their distal tips to make a complete ring. Cinctum contractile, lacking an internal rod-like organelle. Body cylindrical tapering toward oral or aboral body pole. Epistomial disk not free from peristomial border. Macronucleus spherical or cylindrical, micronucleus fusiform.
Type species; Ellobiophrya donacis Chatton & Lwoff. (ref. ID; 3969)
  1. Ellobiophrya brevipes (Laird, 1959) Clamp & Bradbury, 1997 (ref. ID; 7412 redescribed paper)
    Syn; Caliperia brevipes Laird, 1959 (ref. ID; 7412)
  2. Ellobiophrya conviva Clamp, 1982 (ref. ID; 3969 original paper, 4329, 7412)
  3. Ellobiophrya donacis Chatton & Lwoff, 1923 (ref. ID; 3969) or 1929 (ref. ID; 7412) reported author and year? (ref. ID; 191)
  4. Ellobiophrya oblida Naidenova & Zalika, 1969 (ref. ID; 7412), (Naidenova & Zalika) n. comb. (ref. ID; 3969)
    Syn; Clausophrya oblida Naidenova & Zalika (ref. ID; 3969)

Ellobiophrya brevipes (Laird, 1959) Clamp & Bradbury, 1997 (ref. ID; 7412 redescribed paper)

Synonym

Caliperia brevipes Laird, 1959 (ref. ID; 7412)

Descriptions

Light microscopy: Expanded individuals are cylindrical with an unreflected peristomial lip. A slight groove is all that demarcates the peristomial region from the body of the ciliate. A short infundibulum ends at the cytostome, approximately one-fourth of the distance from the peristome to the aboral end of the body. The ampulla is long and slender, tapering smoothly into the cytopharynx. These observations agree with Laird's (1959) original description of the species. The peristomial lips of E. conviva (Clamp, 1982) and E. donacis (Chatton & Lwoff, 1929) resemble the peristomial lip of E. brevipes in being unreflected when expanded, and E. conviva and E. brevipes are also very similar in overall body shape. Ellobiophrya oblida differs from E. brevipes in both characteristics, being widest at its peristome with a thickened peristomial lip that appears reflected in an illustration of the living organism, but is not explicity described as such in the text of its description (Naidenova & Zaika 1969). As Laird observed, the pellicle of living E. brevipes appears smooth when examined by high dry objectives, but closely spaced, faint pellicular striae in fixed and stained individuals are visible by oil immersion objectives, as they are in E. conviva (Clamp, 1982) and E. donacis (Chatton & Lwoff, 1929). By contrast, the pellicular striae of E. oblida are described as prominent (Naidenova & Zaika 1969). The long, flattened macronucleus of E. brevipes is oriented more or less parallel to the long axis of the organism. The oral end of the macronucleus is slightly curved in fixed individuals. The aboral end is larger than the rest of its length and is marked with deep, irregular grooves. This macronuclear shape and orientation are identical to those of E. conviva and E. oblida (Clamp 1982; Naidenova & Zaika 1969). The oral infraciliature of E. brevipes is divisible into a peristomial part and an infundibular part as in other sessiline peritrichs. The peristomial part consists of an outer band of kinetosomes, the polykinety, and an inner band of kinetosomes, the haplokinety, which parallel one another throughout their length. The bands originate on the epistomial disk and continue from there onto the inner edge of the peristomial lip for a total of approximately one and one quarter turns before separating at the infundibulum. They spiral aroud opposite walls of the infundibulum and end at the border of the ampulla (=cytostome). The infundibular part of the haplokinety is a continuation, without visible alteration in its structure, of the peristomial part of the haplokinety. It is accompanied by a germinal row of kinetosomes for approximately half its length within the infundbulum. Inside the infundibulum, the peristomial polykinety transforms into an infundibular polykinetid, designated P1, that is accompanied for part of its length by two other infundibular polykinetids, P2 and P3. Polykinetid 1 is a continuation of the three parallel rows of kinetosomes that form the kinetosomal component of the peristomial polykinety and extends to the edge of ampulla. Polykinetid 2 is formed of three parallel kinetosomal rows that end abstomally just short of the peristomial polykinety and do not merge with it. The rows of P2 terminate adstomal to the adstomal end of P3, noticeably short of the edge of the ampulla, and P2 closely parallel P1 for its entire length. The three short, parallel rows of P3 extend a moderate distance above the abstomal end of P2 and continue abstomally to a point just beyond the abstomal end of P2. A conspicuous, intensely argetophilic cytostomal sphincter (Laird's sideophilic ring (Laird 1959) constricts the passage between the infundibulum and the ampulla. The ampulla itself is small in dimeter, elongate, and almost tubular when not distended with food. It merges with the cytopharynx without any distinct demarcation. The cytopharynx extends almost to the aboral end of the body and recurves before it ends. The aboral end of the body of E. brevipes tapers sharply to the bases of its cinctal arms. Laird (1956) depicted a distinct constriction separating the cell body from the proximal end of the cinctum in hematoxylin-stained specimens. Both protargol and hematoxylin preparations show this constriction, but the living ciliates do not, indicating that it results from contraction caused by fixation. Nothing suggests any kind of physical separation of the cytoplasm of the body proper from the cytoplasm of the cinctal arms. As in other species of Ellobiophrya, the cinctum is a pair of cytoplasmic extensions containing a myoneme nearly circular in section that because of its thick diameter resembles the stalk spasmoneme of vorticellids. The only gap in this myoneme is at the tips of the cinctal arms where a bouton links them. In living ciliates, the bouton was visible as a translucent region between the tips of the cinctal arms. In protargol preparations, the bouton appeared as two opposite hemispheres of argentophilic bodies separated by an unstained region. Since the presence of a bouton linking the cinctal arms is a diagnostic characteristic of Ellobiophrya (Clamp 1982), the presence of a bouton in E. brevipes was the principal justification for moving it to that genus. The dormant scopula is located above the cinctum at the true aboral pole of the body and plays no role in maintaining attachment to the host. A trochal band of barren kinetosomes encircles the body approximately two-thirds other distance between the peristome and the proximal ends of the cinctal arms. (ref. ID; 7412)
  • Ultrastructure:

    Reproduction

    Asexual: In protargol preparations, folding and condensation of the macronucleus signal the beginning of division. The macronucleus collapses along its longitudinal axis and soon assumes a compact shape that contrasts sharply with the elongate macronucleus of interphase trophonts. Unlike the macronucleus, the micronucleus elongates at the beginning of binary fission as it undergoes mitotic division within its envelope. The oral ciliature is resorbed while these early nuclear events take place, and the entire buccal infraciliature is replicated. In addition, the ampulla, cytostomal sphincter, and cytopharynx all disappear at this time. Replication of the buccal infraciliature in E. brevipes occurs as described in other species of sessiline peritrichs (Chatton & Villeneuve 1937; Lom 1964). The daughter infraciliature separate and move into opposing positions after replication, indicating that the final phase of binary fission has begun. At this point, the micronucleus has finished mitosis, and the macronucleus has condensed into a triangluar shape with the apex directed aborally. The nucleoli within the macronucleus are elongate rather than spherical. The peristomial sphincter had condensed, resulting in a smaller peristomial opening than in interphase trophonts. In addition, the peristomial opening of individuals in the late phase of binary fission is retracted into the cell body, in marked contrast to interphase trophonts after fixation. The scopula does not exhibit any visible activity until the late phase of binary fission, but its kinetosomes appear to replicate during the early phase, as evidenced by a noticeable increase in the intensity with which the scopula stains. During cytokinesis, the cleavage furrow bisects the scopula, macronucleus, and peristomial sphincter as it separates the cell bodies of the two daughters. The daughter micronuclei migrate to their aboral position in each future daughter before a cleavage furrow forms, and the middle part of the macronucleus becomes attenuated to a very small diameter before the cleavage furrow passes through it, leaving a mass of macronuclear material concentrated in each future daughter cell. The one region of the parent's cell that does not participate in binary fission, therefore remaining unaffected by cytokinesis, is the cinctum. The entire cinctum is inherited by one daughter, which stays attached in the parent's place. The other daughter becomes a telotroch that does not acquire a cinctum until, presumably, it settles on a host and metamorphoses. As in other ellobiophryids, the telotroch is attached during development to the daughter retaining the cinctum by a short, straight, rigid stalk that passes between the scopulas of the two individuals. This embryonic stalk is larger in diameter and therefore more conspicuous than in E. conviva (Clamp 1982) but less conspicuous than in E. donacis (Chatton & Lwoff 1929). (ref. ID; 7412)

    Ellobiophrya conviva Clamp, 1982 (ref. ID; 3969 original paper, 4329, 7412)

    Diagnosis

    Adult with cinctum composed of two tapered, cytoplasmic extensions of aboral body portion oriented at an angle to long axis of body and joined at their distal ends. Juncture of cinctal limbs marked only by an inconspicuous elliptical structure. Body form cylindrical, either rotund or elongate, and often tapering toward aboral pole. Macronucleus elongate, cylindrical, oriented parallel to long axis of body. Ends of macronucleus at an angle to its main axis; aboral end with deep furrows. Micronucleus fusiform, located near aboral end of macronucleus. Peristomial border indistinctly demarcated from body. Epistomial disk with low, rounded apex. P1 of peniculus entire, ending at cytostome. Row 1 of P1 slightly shorter than its other two rows. P2 approximately equal in length of P3, with all three rows separate from P1 and ending well above the cytostome. Row 1 of P2 slightly longer than its other two rows. P3 curves across the end of P2 to end near the cytostome. All rows of P3 equal in length. Infundibulum ends at 1/3 the distance from peristome; cytopharynx elongate, terminating near aboral end of macronucleus. Telotroch with larval stalk anchored in embryophore of parent. (ref. ID; 3969)

    Descriptions

    The body of ellobiophryids consists of two major regions: the body proper, for which the name soma is proposed here, and the bipartite, ring-like holdfast, for which the name cinctum is proposed. The earlier name for the cinctum, attachment organelle, is inappropriate for two reasons: it is not strictly one organelle but a major part of the body, and it encircles a portion of the host's body, loosely or tightly, rather than attaching to it. The name cinctum (Latin: belt or girdle) describes structure and function more precisely. The soma of ellobiophryids does not differ from the typical peritrich body plan. However, the cinctum, consisting of two slender extensions of the aboral end of the soma which may or may not to be jointed to one another at their tips, is a structure found in no other peritrich group. The only other ciliate to possess a structure which may be called a cinctum is the suctorian Erastophrya chattoni Faure-Fremiet, hypercommensal on Apiosoma piscicola (Blanchard), a peritrich found on the skin of fishes. The soma of E. conviva is cylindrical, often tapering slightly toward the aboral end where the two opposing limbs of the cinctum join it at an angle to its long axis. The surface of the soma is marked with faint transverse annular striae. Some individuals are elongate, others are rotund. The soma often appears slightly flexed near the middle. The aboral tip of the soma is a bulge projecting past the bases of the cinctal limbs. A well-defined circle of dark granules, the scopula, is visible in the center of the aboral pole of silver-impregnated individuals. The adoral region of the soma is bordered by a relatively tall, thin peristomial collar whose separation from the rest of the body is marked only by an indistinct constriction. The epistomial disk has a low, rounded apex. As in other ellobiophryids, the peristomial lip of E. conviva does not completely constrict cover the retracted peristome but leaves a small aperture through which the tips of the peristomial cilia protrude. The haplokinety and polykinety describe approximately one and one-quarter turns together on the peristome before entering the infundibulum, where they separate and make another complete circuit around the wall and end at the cytostome. The elongate cytopharynx opens very near the aboral end of the macronucleus. In the infundibulum, the peniculus consists of the three triple rows of kinetosomes typical of sessiline peritrichs, arranged in a distinctive pattern. The first triple row (P1) remains unbroken for its entire length, ending at the cytostome. The other two triple rows (P2 and P3) are both short and run more or less parallel to the terminal portion of P1. Considerably above the level of the cytostome, P2 ends. Curving across the end of P2, P3 terminates at an acute angle to the end of P1. In P1, the first row of kinetosomes (counting toward P2) is shortest, the second is slightly longer, and the third is the longest. In P2, the first kinetosome row is slightly longer than the other two. All three rows of P3 are equal in length. As in other peritrichs, the infundibular portion of the haplokinety is found opposite the peniculus and consists of a single row of kinetosomes that ends at the cytostome. It is accompanied, as usual, by the germinal row of kinetosomes (G) for part of its length. The infraciliature of the trochal band is clearly visible in adult E. conviva impregnated with protargol. It consists of a single row of kinetosomes encircling the soma at approximately two-thirds the distance from the peristome to the aboral body pole. The macronucleus is a long, thick cylinder with both ends bent at an angle to its long axis. Its length cannot be determined due to its irregular, variable shape but appears to approach that of the soma. The aboral end of the macronucleus is marked with deep grooves that converge at a single point, similar to the fossa with radiating diverticula found on the surface of the macronucleus of E. donacis (Chatton & Lwoff, 1929). The micronucleus is an oval or fusiform body set into a slight recess in the surface of the aboral end of the macronucleus. In stained preparations, it is surrounded by a sharply defined clear area. The cinctum is made up of two slender, opposing extensions of the aboral portion of the body that are cemented to one another at their tips. The point at which the two extensions or limbs are joined is distinguished only by an elliptical area, most clearly visible in protargol preparations, that stains more lightly than the surrounding cytoplasm. Each cinctal limb consists of two portions, a thick basal section which tapers sharply away from its origin and a band-like distal portion. The two parts are always demarcated from one another by a slight constriction at the midpoint of the limb. The thickness of the distal part of the limb cannot be measured with accuracy, but its optical cross section is approximately 3 um thick. The cinctum grips the tentacle of the host firmly, so that the body of the ciliate remains always in the same position on the host (i.e., on the inner side of a tentacle with its oral end facing toward the tentacle's tip). It stained preparations, the portion of the host's tentacle encircled by the cinctum often appears constricted by the strength of the ciliate's grip. The cinctum is thus apparently capable of contraction to some degree. Contractions are not obvious in living ciliates, but the ridged appearance of the cinctal limbs in many fixed individuals suggest contraction has taken place. Also, darkly staining bands that are probably myonemes are visible in the limbs of silver-impregnated individuals. Contractility of the cinctum may be necessary to help the peritrichs maintain their hold on the host, since they are in an exposed position on an animal that often retracts suddenly and forcefully. Reproduction in E. conviva resembles the process described for E. donacis (Chatton & Lwoff 1928, 1929). The initial stages of binary fission were not observed in E. conviva, but individuals in later stages were seen. The scopula appears to be the last point of attachment between parent and offspring in the terminal stage of division when a thin, twisted, dark strand can be seen connecting the scopular appears of each in protargol preparations. Telotrochs of E. conviva secrete a temporary stalk, like the larval stalk described in E. donacis, that attaches them to the parent during the period between completion of division and their liberation. The embryophore, a raised area on the aboral surface of the body of E. donacis in which the embryonic stalk is anchored, is likewise present in E. conviva. The larval stalk dose not attain the length and thickness in E. conviva that it does in E. donacis. It is quite difficult to see because most of its length is buried within the embryophore of the parent. Telotroch of E. conviva are similar to those of E. donacis. They are cylindrical to pyriform or almost globular in shape, with the widest portion of their body adoral to the trochal band of cilia. As in E. donacis, the scopula of E. conviva telotrochs appears to be displaced slightly away from the aboral body pole. However, the numerous short cilia observed by Chatton & Lwoff on the aboral pole of the telotroch of E. donacis were not visible on E. conviva telotrochs. Conjugation was not observed in E. conviva, nor has it been observed in any ellobiophryid species. (ref. ID; 3969)

    The elongate body of E. conviva usually is oriented on the host with its peristome facing the base of the tentacle to which it is attached. Most frequently, it lies at an acute angle to the tentacle because the cinctal arms are placed asymmetrically in relation to the long axis of the body. The scopula is not visible in living individuals but appears as a darkly staining disk in protargol preparations. The cinctum visibly constricts the host's tentacle. Each arm of the cinctum is a direct continuation of the body that tapers abruptly into a long, slender strap. Protargol preparations show darkly stained bands of myonemes that run the length of each cinctal arm. The cinctal arms are linked by the bouton that appears in protargol preparations as a clear, oval area surrounded by darkly stained material. In living individuals, a faint, diagonal groove encircles the cinctum where the cinctal arms meet. It marks the location of the bouton, which is otherwise invisible when unstained. The bouton firmly bonds the cinctal arms. Fixed individuals were dislodged from tentacles only when an arm was snapped by mishandling or pressure from a coverslip. Breakage never occurred at the bouton, only in the middle of an arm. (ref. ID; 4329)

    Type locality

    U.S.A., North Carolina, Carteret County, Newport River at eastern shore of Radio Island, 1.15 miles (1.8 km) WSW Beaufort. (ref. ID; 3969)

    Type-host

    Bugula neritina (L.) (ref. ID; 3969)

    Type specimens

    Four slides of type-specimens have been deposited in the International Protozoan Type Slide Collection, National Museum of Natural History, Washington, D.C. Two of these, one protargol and one Heidenhain's iron hematoxylin preparation, are designated syntypes. The others, both hematoxylin preparation, are designated as paratypes. Additional paratypes are in the author's collection. (ref. ID; 3969)

    Ellobiophrya donacis Chatton & Lwoff, 1923 (ref. ID; 3969) or 1929 (ref. ID; 7412) reported author and year? (ref. ID; 191)

    Descriptions

    This bizarre ciliate commensal of the marine lamellibranch mollusc Donax vittatus has been the sole representative of its genus. (ref. ID; 3969)