radiolaria - rads_cenozoic - Collozoum caudatum radiolaria - rads_cenozoic - Collozoum caudatum

Collozoum caudatum


Classification: rads_cenozoic -> Sphaerozoidae -> Collozoum -> Collozoum caudatum
Sister taxa: C. amoeboides, C. caudatum, C. coeruleum, C. contortum, C. fulvum, C. hertwigi, C. longiforme, C. minus, C. moebii, C. radiosum, C. vermiforme

Taxonomy

Citation: Collozoum caudatum Swanberg & Anderson 1981
taxonomic rank: species
Basionym: Collozoum caudatum Swanberg & Anderson 1981

Catalog entries: Collozoum caudatum

Original description: Diagnosis. Colony cylindrical, markedly elongated from 3 to 200 cm long, approximately 1 cm diameter; characteristically with a thick occasionally mildly crenated, translucent, and colorless gelatinous sheath surrounding a core of glistening alveoli and opalescent to lightly purplish central capsules, each with many zooxanthellae. Central capsules spherical or ovate, 100 to 300 µm diameter. Colony almost always has a drooping gelatinous tail-like structure at each end containing shells of digested prey and other waste products.
Holotype. The holotype specimen was collected by Neil Swanberg at 1524 local time on 21 March, 1977 at 6°47'N, 38°42'W (Sta. 561, surface temperature 26.3°C). A portion of the large colony was fixed for electron microscopy, a portion will be deposited with the U.S. National Museum.
Description
Colony morphology. The cylindrical colonies of Collozoum caudatum previously presented as Collozoum sp. A (SWANBERG, 1979), can attain a length of at least 2 m, although shorter colonies are more common. Large colonies are occasionally toroidal or have more complicated (branched) structures, probably generated by the fusion upon contact of separate parts of a colony. Such fusion was observed within and between colonies when several colonies were confined in the laboratory. Colonies less than 10 cm long appeared especially plump and sausage-like (Fig. 1A) due to their large diameter. There is a core of central capsules, zooxanthellae, and alveoli (Fig. 1B) surrounded by a thick coat of dense, glutinous, translucent gelatin (Fig. 1A). The diameter and opacity of the core appears to increase with increasing cell number and age of the colony.
The rhizopodia which form a dense network radiating from the central capsules are visible even under low magnification (Fig. 1B). These penetrate the gelatinous coat and may or may not form a fringe at the colony surface, depending on whether the organism is extending its rhizopodia into the environment. If the rhizopodial fringe is not extended, the colony border is abrupt. In one specimen, which was closely examined under Nomarski optics, we observed two linear aggregations of rhizopodia running along the 1 to 2-cm extent of the colony segment. The rhizopodia appear to control the distribution of the symbiotic algae. When a colony is placed in the dark, the algae are drawn close to the central capsules; when returned to the light, they are redistributed within the gelatin of the colony.
A tail-like strand of gelatin containing rhizopodia usually dangles from each end of the colony. The strands (Figs 1A, C) are composed mostly of undigested prey debris, especially the empty loricae of tintinnids and shells of larval or juvenile molluscs. As the 'fecal' strands elongate, pieces drop from them carrying away the undigested debris. Very rarely did fecal strands emerge from a lateral surface of a colony, though it was not unusual to find more than one stub or start of a strand at the end of a colony.
Cell morphology. The central capsules are large, 100 to 300 µm diameter, opalescent to purplish with a few oil droplets in smaller cells. One massive central capsule oil droplet occurs in larger cells. Central capsules of young colonies usually appear amber in color due to the abundant algae. There were more algae per cell in this species than in any other colonial radiolarian yet described. For three measured specimens the average number of central capsules in a centimeter of colony length was 58, with 311 algae per central capsule (range 250 to 350 algae per central capsule; 40 to 70 central capsules per centimeter). Most colonialradiolarians have approximately 10 to 20 algae per centralcapsule (BRANDT, 1885; ANDERSON, 1980). In many colonies the cells had acquired a noticeable purple color. Under the light microscope this appeared as an array of circular platelets (3 to 4 µm diameter) on the near surface of the central capsule (Fig. 1D).
Fine structure. A segment of a cell near the periphery of the central capsule contains radially arranged lobes of cytoplasm intertwined with one another and interconnected to form a network (Fig. 2A). A tangential section in a plane nearly perpendicular to the long axis of the lobes exhibits their arrangement and lateral connections (Fig. 2B). The plasma membrane surrounding the cytoplasmic lobes delimits a meandering cisternal space of varying width (C in Fig. 2B) that ramifies among the lobes of the cytoplasmic network. This reticulated cytoplasmic organization is present throughout the central capsule as determined by a sequential series of sections taken through an entire cell. Nuclei (Fig. 2C) approximately 20 µm in diameter occur within the lobes and are surrounded by a thin layer of cytoplasm. Each nucleus is surrounded by a double-membrane envelope typical of many eucaryotic cells. The number of nuclei within a cell varies and appears to increase as the cell reaches reproductive maturity. When the nuclei are not numerous, they occur largely near the central part of the cell and contain a fine fibrillar network of chromatin. During proliferation, they spread throughout the cytoplasm and the chromatin may condense into cord-like masses such as we have observed in one specimen. Intermediate stages can be observed with condensed masses of chromatin (Fig. 2D).
Each of the interconnected lobes (Fig. 3A) contains mitochondria (M) with tubular cristae as are frequently found in protozoans, single membrane-bound organelles that appear to be peroxisomes (P) containing a finely granular matrix with an occasional denser osmiophilic granule; a large number of Golgi bodies (G), smooth endoplasmic reticulum, and vacuoles of varying size. Large vacuoles (ca. 4 µm diameter) occur at the periphery of many of the lobes (Fig. 3B) and frequently contain electron-dense granules (ca. 2 µm diameter) that appear to have the same approximate size and are distributed among the vacuoles in the same pattern as the near-surface, pigment granules observed with the light microscope in whole living cells (Fig. 1D).
The endoplasmic reticulum in the intracapsular cytoplasmic lobes is dilated in some regions and contains a dense deposit of osmiophilic, fibrillar substance arranged in compressed whorls (Figs 3C, D, 4A). The morphology of the dense, fibrillar bodies varies from spindle-shaped to multi-lobate (Fig. 3D). Occasional interconnections are seen between the membranous envelopes surrounding adjacent dense bodies, but on the whole, it appears that the fibrillar bodies are not part of a single, membrane-bound organelle. The endoplasmic reticulum in the vicinity of the fibrillar bodies, and sometimes connected to them, contains a finely fibrillar material resembling the finely dispersed fibrils at the perimeter of the dense bodies (Fig. 4B). The chemical composition and function of the fibrillar material is not known. No evidence of this substance has been found in the extracapsular cytoplasm.
The periphery of the central capsule (Fig. 3B) is surrounded by the central-capsule wall membranes (CW, Figs 3B, 4C), perforated by cytoplasmic strands called fusules (ca. 400 nm diameter) first described by CACHON and CACHON (1972) in solitary species. The fusules provide continuity between the intracapsular and extracapsular cytoplasm. The cisterna within the double membranes (arrow, Fig. 3B) contains a thin deposit of an osmiophilic substance. The organization of the capsular wall membranes and fusules is shown in greater detail in Fig. 4C. The inner membrane (I) of the capsular wall envelope is continuous with the plasma membrane surrounding the proximal segment (P) of the cytoplasmic strand in the fusule and continues as the plasma membrane surrounding the intracapsular cytoplasmic lobes (arrow, Fig. 4C). The outer membrane of the envelope (O) is continuous with the distal portion (D) of the fusule that connects to the rhizopodial network surrounding the central capsule. In all of the sections we have observed, the fusules project outward, forming a series of raised tubules on the surface of the central capsule (asterisk, Fig. 3B). A dense cone of organic substance occurs within the fusule at the junction of the extracapsular and intracapsular cytoplasm and projects into the rhizopodial cytoplasm. High magnification images of longitudinal sections through the dense cone show little internal organization, although there is occasional evidence of fine filaments lying parallel to its long axis. Vesicles sometimes occur in the cytoplasm of the proximal fusule segment and the dense matrix of the cone (Fig. 4C), thus suggesting that it is sufficiently open to allow penetration by cytoplasmic particles.
The extracapsular cytoplasm forms a vacuolated layer near the surface of the central capsule and gives rise to rhizopodial strands in a network penetrating throughout the gelatinous sheath of the colony. Food vacuoles, digestive vacuoles in various stages of development, and waste vacuoles appear in the extracapsular cytoplasmic layer (Fig. 4D) and sporadically within the cytoplasmic network. Osmiophilic granules of unknown composition occur throughout the extracapsular cytoplasm.
Zooxanthellae (Fig. 4E), exhibiting typical dinoflagellate fine structure, occur within membrane-enclosed spaces in the rhizopodial network. In some cases, the zooxanthellae are dividing and appear in late telophase with two daughter cells closely adhering to one another within a common vacuolated space. Rhizopodial strands containing vacuoles, mitochondria, electron opaque granules, reserve bodies, and vesicles penetrate the gelatinous sheath which exhibits a finely osmiophilic network (Fig. 4F).

Distribution. Collozoum caudatum was found in 107 of 302 stations for which presence and absence data were collected. Most of these stations were on the Atlantic equator or in the vicinity of the Gulf Stream (Fig. 5); in addition it was found at 16 of 29 stations between 03°0'S and 02°0'N at 55°30'E in the Indian Ocean near the Seychelles during La Curieuse 7601 to 7605. It was rarely found at or near the surface, but usually 5 to 30 m deep; we rarely dive deeper than 30 m.
Stations: 417, 426, 427, 458,460, 467, 469 to 476, 478 to 481,483, 497, 514, 519, 522, 523, 527,528,555,559 to 561,564, 567,568,574, 577,582, 583,585,587 to 589,591 to 594, 596, 608,610, 612,613,624 to 631,643,737,740, 752, 753,755,757,759,761 to 767,769 to 771, 773, 774, 776, 778, 780, 783 to 791,793, 807, 809 to 815, 822, 824, 828, 829, 832, 834, 836 to 839.
Solitaries: 404, 424, 473, 528, 740, 770, 829.

Comments. We were unable to observe the ontogenetic development of C. caudatum. However, examination of 72 preserved specimens identifiable by their colony morphology as C. caudatum revealed several forms that can be assembled into a developmental sequence resembling the developmental stages of Thalassophysa sanguinolenta Haeckel. These stages were formerly thought to be separate species of Collozoum (BRANDT, 1902; HOLLANDE and ENJUMET, 1953).
We have collected a number of solitary radiolaria possessing tail-like structures and otherwise resembling the colonial C. caudatum. These could be the monozoic or solitary developmental precursors of the colonial form. The fine structure of one solitary radiolarian specimen was examined. Only a brief description is presented, as we plan to give a more thorough analysis of its structure and possible ontogenetic relation to the colonial form in a later report when additional laboratory data have been obtained. The solitary, large central capsule is surrounded by a thick, organic capsular wall (1 µm thick) containing fine fissures and fusules. The densely granular intracapsular cytoplasm is arranged in closely packed lobes separated by narrow, meandering cisternae. Numerous mitochondria with tubular cristae occur at the periphery of the central capsular cytoplasm but are less abundunt near the center of the cell. Large, electron-lucent vacuoles (15 µm diameter) become increasingly abundant toward the center of the central capsular cytoplasm. Occasional dense, fibrillar bodies resembling those observed in the colonial specimens were enclosed in dilated segments of the endoplasmic reticulum. The nucleus, near the center of the cell, is surrounded by a double-membrane envelope and contains a fine fibrillar network of chromatin. The extracapsular cytoplasm formed masses of vacuolated cytoplasm and a network of rhizopodial strands enclosing dinoflagellate symbionts, resembling those observed in the colonial form.
Three specimens we believe represent a transition from a solitary stage to an early stage in the colonial development were elongate colonies with few cells. The colonies were very delicate and transparent, and the gelatin was not very dense. The prolate spheroidal central capsules form a single row along the length of the colony. To the naked eye in the field this gives the colony the appearance of a hyphenated line. In two other specimens, possibly representing a more advanced stage of central capsule proliferation, we found serpentine central capsules as in Collozoum serpentinum Haekel and Collozoum vermiforme HAECKEL (1887). These clearly are not C. vermiforme or C. serpentinum as the thick gelatinous sheath with terminal fecal strands and other morphological details resemble C. caudatum. A third colonial form (22 specimens) had discrete central capsules that were usually oblong or spherical (100 to 300 µm diameter) with several vesicular structures (presumably oil droplets) in them. The fourth form and presumably most mature stage in the sequence (29 specimens) had usually spherical capsules between 250 and 300 µm in diameter dominated by a large central oil droplet. In our electron microscopic observations, moreover, we have observed that prolate central capsules contain small lipid droplets and fewer nuclei than the more spherical central capsules, which contain a large centrally located lipid reserve body surrounded by densely packed cytoplasmic lobes containing numerous closely spaced nuclei resembling those observed in reproductive stages of Sphaerozoum punctatum Müller (ANDERSON, 1976b). Several specimens seemed to overlap between stages in one feature or another. Dividing cells were seen in the third and fourth forms, as were pigmented granules. It is our impression that pigment granules were more common or more prominent in the latter stages.
We consider the above forms as conspecific on the basis of the microscopic structure of the cells (aside from shape) and of the distinctive colonial morphology. We have found other radiolarian colonies, previously described as Collozoum sp. B (SWANBERG, 1979), that strongly resembled C. caudatum in gross cell morphology but differed in colony shape. They are lemniscal (ribbon-shaped), usually from 50 to 100 cm long, 2 to 3 cm wide, and 5 mm thick. We suspect that they may be a form of C. caudatum as we have observed one normal C. caudatum colony alter its gross morphology to a band-shaped structure when confined overnight in laboratory culture. The cells resemble forms three and four above, but we have never seen them with pigment granules nor do they possess fecal strands on the colony. We do not have any of these fixed suitably for electron microscopy and thus cannot be certain that they are or are not the same species; however, most light micrographs (in vivo) and preserved cells are nearly indistinguishable from those of C. caudatum. They are much more difficult to collect intact than 'normal' C. caudatum because their gelatin is softer and they have a tendency to fragment readily on capture. This is apparently caused by intense contraction of the peripheral rhizopodia at regular intervals along the margin of the colony.
Other observations suggest a fair amount of control over colony shape. When colonies of C. caudatum are encountered in situ they are often relatively flaccid or relaxed. After collection, the length of the colony usually decreases substantially and the colony becomes firmer and more resistant to mechanical deformation. Such a change might be effected by contraction of the rhizopodial system. More radical changes also occurred; some colonies greatly reduced their diameter in a manner resembling a single peristaltic wave, presumably concurrently discharging the alveolar contents. In other species in which this behavior has been reported (SWANBERG, 1979) the entire colony loses buoyancy and sinks to the bottom of the jar or vessel. When such shrinkage occurred in one specimen of the first form (the 'hyphenated' stage), the rhizopodia were contracting into discrete dense masses near the large cells and squeezing the alveoli to the perimeter of the colony. We also observed a number of young vegetative colonies (form three) in which the central capsules were aggregated in groups along the length of the colony; to the unaided eye these resembled the 'hyphenated' stage. After several hours in the laboratory the groups dispersed and the cells were more evenly distributed through the colony.


Discussion. The genus Collozoum Haeckel 1862 was erected to include those colonial radiolaria that do not form siliceous skeletons. This is probably a somewhat artificial category (HOLLANDE and ENJUMET, 1953), but until more is understood of the developmental relationships between solitary and colonial sphaerocollinid radiolaria it must suffice. The absence of the morphological intricacy found in the shell-bearing species has made the genus Collozoum difficult to distinguish at the species level. Many of the early descriptions are inadequate because they are based solely on preserved material and emphasize characters of dubious taxonomic significance (SWANBERG and HARBISON, 1980). We concur with BRANDT (1905) that by observation of living material many species can be easily recognized. However, there are probably many synonymous species that are merely stages of the solitary and colonial Sphaerocollina, both shelled and shell-less. Until the life cycles are better understood these questions cannot be resolved.
In an attempt to avoid redundancy in systematics, we have sought to identify as many stages and forms as possible on the basis of structure. The figures of BRANDT (1902) and HOLLANDE and ENJUMET (1953) showing the developmental stages of Thalassophysa sanguinolenta show considerable resemblance to similar stages in C. caudatum, though their scale and colony morphology differ. We suggest that the solitary form described in this paper develops analogously to that of T. sanguinolenta, Thalassophysa spiculosa Haeckel and Thalassophysa pelagica Haeckel. In these species the spherical solitary central capsule becomes lobate, the lobes elongate enormously and then break up into central capsules, which enlarge and divide. In C. caudatum the 'hyphenated' stage may represent the breaking up of the elongate central capsule. The serpentine stage could represent further elongation of the capsules formed by the first divisions. The cells would continue to divide until they form oval or spherical central capsules yielding swarmers at maturity. No one yet knows the fate of the swarmers. It is appealing to think that they form solitaries directly, but there is no evidence for this. Laboratory experiments will be necessary to confirm such hypothetical relationships and to explore early development of the flagellated swarmers.
Our hypothesis that the solitary form is an early ontogenetic stage of the colonial form is strengthened by the similarities in fine structure, particularly the presence of the dense fibrillar bodies in both forms. We have assigned the colonial form to the genus Collozoum largely on the basis of gross morphology, but the fine structure also supports the classification. Both C. caudatum and Collozoum inerme Haeckel (ANDERSON, 1976) have radially arranged, anastomosing intracapsular cytoplasmic lobes separated by narrow cisternae. The cytoplasmic lobes terminate directly at the capsular wall membrane and connect to the fusules without an intervening thin layer of cytoplasm lying next to the inner surface of the capsular wall membranes as occurs in Collosphaera globularis Haeckel (ANDERSON, 1978). We do not know at present how the cytoplasmic organization changes during maturation and reproduction in either C. caudatum or C. inerme and further research is planned to elucidate these events. However, both C. caudatum and C. inerme have multi-nucleated central capsules. The nuclei, in their early stages at least, contain a fine fibrillar chromatin network and have internal microtubules attached to a persistent nuclear membrane. The fine structure of C. caudatum is clearly distinguished from that of C. inerme by the presence of the dense, fibrillar bodies and the occasional dense osmiophilic granules in the vacuoles at the perimeter of the intracapsular lobes.
Coliozoum caudatum also resembles C. longiforme in the size and general shape of the colony. It is easily distinguished from C. longiforme by the thickness and consistency of the jelly envelope, the size and appearance of the central capsules, and the formation of the fecal strand. HAECKEL (1887) described 13 species of Collozoum from the Challenger material. Although most of his sparse descriptions were based primarily on central capsule shape, not a reliable character, three of them are similar enough to C. caudatum to warrant our consideration. Collozoum nostochinum Haeckel had 200 to 300 oil droplets and opaque spherical central capsules 300 to 500 µm in diameter, distended with red pigment granules. Collozoum volvocinum Haeckel had l0 to 30 large oil droplets and opaque spherical central capsules containing densely packed masses of dark pigment. Collozoum ovatum Haeckel was ellipsoidal with one single oil globule. Its cell diameter (major and minor axes, respectively) was 200 to 300 µm and 100 to 150 µm. The first two of these species are in Haeckel's subgenus Collodinium including radiolaria with "form of the central capsules spherical or subspherical, never polyhedral, ellipsoidal or cylindrical". Technically this would exclude C. caudatum from the group, but we recognize that central capsule shape alone is insufficient information to identify a species of Collozoum. Even so, we have difficulty forcing our species into either description. We have never seen C. caudatum with so many oil droplets, nor have we ever seen the central capsules opaque. Both species appear to be described on the basis of a single specimen or station. C. ovatum could be C. caudatum, but Haeckel's description is completely inadequate to determine whether it is or not. None of the other species of Collozoum comes so close as these to our species, nor have any previous authors mentioned the tail-like strands observed on our species. This raises the question of how the early authors could have missed such a widespread species. Although C. caudatum was seldom abundant in our stations, it was widely distributed in the Atlantic and is certainly present in the Indian Ocean. It is possible that it was collected by the nineteenth century expeditions, but it could have been damaged by nets and fixation and rendered unrecognizable as a radiolarian. This could result from the rupture of the massive but fragile gelatinous coat of the radiolarian. C. caudatum is unique among known radiolaria in the abundance of gelatin surrounding the colony. The sheer quantity observed in C. caudatum, and to a lesser degree in other species, highlights the question of how precursors for the gelatinous coat are stored and mobilized for synthesis and deposition. The dense fibrillar bodies may be a precursor pool or condensed form of the mucoid gelatin that is deposited outside of the central capsule. The whorled appearance of the fibrillar substance is similar to the mucous content of secretory granules in planktonic foraminifera (ANDERSON and BÉ, 1976), which strengthens the evidence that the whorled masses may be gelatin precursors. Since no evidence of Golgi secretory bodies or abundant masses of endoplasmic reticulum have been observed in the extracapsular cytoplasm of most radiolaria examined so far, we believe the gelatin precursor could be synthesized in the central capsule and may be transported to the extracapsular cytoplasm in vesicles passing through the fusules as shown in Fig. 4C.
The large colonies of C. caudatum are also unique among the radiolaria in their degree of organization. This is best illustrated by the formation of the fecal strand at the poles (ends) of the colony. We have not observed movement of waste material from the center of the colony to the poles, but we have seen movement of waste material from cells near the poles into the tails. Transport is most likely by the rhizopodia. The trunks of rhizopodia running the length of the colony could transport prey remains from the center of the colony to the poles. Such a system would require some functional differentiation between rhizopodia for prey capture and those for waste disposal and may also provide a mechanism for distributing the products of predation among all the cells of the colony.
There may be intercellular organization by rhizopodial connection between cells or among groups of cells in the colony. The aggregation of central capsules of young vegetative colonies into periodic linear groups suggests that the cells in the colony are not randomly distributed. The cells may be organized into groups to more efficiently utilize food from large particles or each group of central capsules may function as a physiological unit. The latter might be the case if the large central capsules of the 'hyphenated' stage were to divide without separation of the remaining rhizopodial connections. General rhizopodial contraction, drawing the central capsules together and reducing the length of the colony, seemed to occur simultaneously throughout the colony. However, shrinking of the colony diameter, accompanied by loss of buoyancy, occurred as a single slow peristaltic wave, usually starting somewhere in the midst of the colony and proceeding towards each end. Thus the contractile stimulus was somehow relayed along the colony length.
We have shown that colonies of C. caudatum control the internal distribution of central capsules, algae, and waste prey particles and to some extent determine colony texture and size. They can change their buoyancy and shape. Thus they do not appear to be amorphous blobs of gelatin containing scattered and uncoordinated cells, but highly organized colonial structures exhibiting signs of primitive differentiation of function for apprehending prey, distributing nourishment, and discarding waste.

Description

Biogeography and Palaeobiology

Biostratigraphic distribution

Geological Range:
Last occurrence (top): Extant. Data source:
First occurrence (base): within Recent modern (0.00-0.00Ma, base in "Holocene" stage). Data source:

Plot of occurrence data:

References:

Swanberg, N. R. & Anderson, O. R. (1981). Collozoum caudatum sp. nov.: A giant colonial radiolarian from equatorial and Gulf Stream waters. Deep-Sea Research. 28A(9): 1033-1047. gs


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Collozoum caudatum compiled by the radiolaria@mikrotax project team viewed: 26-6-2024

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