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EVIDENCE OF BINARY DIVISION IN MATURE CENTRAL CAPSULES OF A COLLOSPHAERID COLONIAL RADIOLARIAN: IMPLICATIONS FOR SHELL ONTOGENETIC PATTERNS IN MODERN AND FOSSIL SPECIES

O. Roger Anderson and Shyam M. Gupta

Plain Language Abstract

Colonial radiolaria are among the largest and most elegant of radiolaria, consisting of a clear gelatinous envelope (sometimes several centimeters in diameter) enclosing numerous spheroidal central capsules, each surrounded by an elaborate siliceous shell in skeletal-bearing species. A few entire colonies are illustrated at: http://palaeo-electronica.org/1998_2/boltovskoy/fig1c.htm. For illustrations of the isolated shells of colonial radiolarians, see the entries in the family Collosphaeridae of the order Spumellaria in the 'Identification of species' section of Boltovskoy's article at: http://palaeo-electronica.org/1998_2/boltovskoy/issue2 .htm. Abundances of colonies can reach several hundred per cubic meter in the oceans, and the siliceous skeletons are widely represented as microfossils in marine sediments. While much attention has been given to their sedimentary distribution and abundance over geological time, less is known about how their skeletons are formed and to what extent mature central capsules are capable of dividing to increase the size of the colony.

It is known that during the development of many species, the central capsules divide repeatedly before all of them secrete a skeleton nearly simultaneously. This is called simultaneous central capsule proliferation and maturation. Moreover, non-skeletal bearing species can increase their size and number of central capsules through binary fission (splitting into two) of the central capsule. Do skeletal-bearing central capsules divide or is the enclosing skeleton the final stage of development?

Data reported here from fossil shells and living colonies collected in the Sargasso Sea indicate that in the genus Acrosphaera that we have been able to observe, mature central capsules can reproduce by a fission process known as budding. A second shell is sometimes produced at one side yielding an hour-glass shape in fossil specimens. Likewise, similar hour-glass shaped, or separated, paired-shells are observed in living individuals. Putative early stages of budding in living individuals have also been observed as bud-like protrusions of the central capsule cytoplasm. This would indicate a "successive" shell deposition as the colony matures, with additional central capsules added at later times during subsequent proliferation within the gelatinous envelope. This may be significant in understanding how colonial radiolaria proliferate asexually and help to explain the relatively large size and high abundances of colonial radiolaria in the surface water of some oceanic locations.

Glossary (in order of appearance, in abstract and article):

Central capsule: In an individual living radiolarian, a dense central mass of protoplasm which includes the nuclear material, as well as constituents important in respiration, digestion and food storage. A central capsular membrane separates this intracapsular material from the extracapsular protoplasm. In a colonial radiolarian, each central capsule defines a single organism, and the extracapsular protoplasm holds the central capsules (with their shells, when present) together to form the colony.
Diagenesis: Chemical change after sedimentation.
Ontogenesis: The course of development of a single organism.
Phylogeny: The evolution of a genetically related group of organisms.
Polycystinea: Radiolaria in which the skeleton is of simple opaline silica, not of a combination of silica and organic material as it is in the Phaeodaria.

Resumen en Español

Evidencias de división binaria en cápsulas centrales maduras de un radiolario colonial collosfèrido: implicaciones en la comprensión de las pautas ontogenéticas de la concha de especies actuales y fósiles

Se presentan evidencias, a partir de especies vivientes y conchas fósiles, de que las cápsulas centrales maduras con conchas del radiolario colonial Acrosphaera pueden producir cápsulas centrales y conchas hijas por fisión binaria. Estos datos indican que, al menos en los radiolarios collosfèridos coloniales, la proliferación de cápsulas centrales puede tener lugar después de la maduración, lo que explica el rápido crecimiento de la biomasa y del tamaño de la población en respuesta a las condiciones ambientales favorables. Esto también apoya las evidencias anteriores de que las cápsulas centrales de los radiolarios coloniales sin concha pueden proliferar por fisión binaria. Estas observaciones también amplían nuestro conocimiento de la pauta de silicificación y formación de la concha, incluyendo dos posibilidades: (1) la idea habitual del "depósito simultáneo de conchas", en la que todos los esqueletos se depositan casi al mismo tiempo, tras las divisiones múltiples de la cápsulas centrales sin esqueleto y (2) la del "depósito sucesivo de conchas" en la que las cápsulas centrales maduras con conchas dan lugar a otras adicionales mediante fisión binaria retardada. Estas observaciones tienen interesantes implicaciones en las dinámicas de los ciclos vitales de los radiolarios en ambientes oceánicos modernos y del pasado.

Palabras clave: fisión binaria, radiolarios coloniales, ecología, ontogenia del caparazón

 

Résumé en Français

Évidences d’une division binaire dans les capsules matures d’un radiolaire colonial collosphaeride: implications pour les patrons ontogénétiques des coquilles d’espèces modernes et fossiles.

Des évidences de coquilles fossiles et d’espèces vivantes du radiolaire colonial Acrosphaera indiquent que les capsules centrales matures peuvent produire des capsules centrales filles par fission binaire. Ces données indiquent que du moins chez les radiolaires coloniales collosphaerides, la prolifération des capsules centrales peut se produire après la maturité et peut expliquer les croissances rapides de biomasse et de population en réponse à un environnement favorable. Ceci rajoute aux évidences antérieures que les capsules centrales de radiolaires coloniales sans coquille peuvent se reproduire par fission binaire. De plus, ces observations augmentent nos connaissances au niveau des patrons de silicification et de formation des coquilles pour inclure deux possibilités: (1) la pensée courante du "dépôt simultané des coquilles", selon lequel les squelettes sont formés en un temps à la suite de divisions multiples de capsules centrales sans squelettes, et (2) la "déposition successive des coquilles", selon lequel les capsules centrales matures avec coquilles se reproduisent par fission binaire tardif. Ces observations ont des implications intéressantes pour la dynamique des cycles de vie des radiolaires dans les environnements marins actuels et anciens.

Mots clés: Fission binaire, radiolaires coloniales, écologie, ontogénèse des coquilles

 

Deutsche Zusammenfassung

Hinweise auf Teilung in reifen Zentralkapseln collosphaerider kolonialer Radiolarien: Folgerungen für ontogenetische Abläufe bei heutigen und fossilen Arten

Aufgrund von Beobachtungen an fossilen und lebenden Arten der kolonialen Radiolariengattung Acrosphaera werden Belege dafür präsentiert, dass reife Zentralkapseln mit Schalen Tochterkapseln und Schalen durch Teilung erzeugen können. Die Beobachtungen zeigen, dass zumindest bei kolonialen collosphaeriden Radiolarien eine Vermehrung der Zentralkapseln nach der Reifung stattfinden und unter günstigen Umweltbedingungen zur raschen Zunahme von Biomasse und Populationsgrösse führen kann. Damit werden bestehende Belege für Teilung von Zentralkapseln bei kolonialen Radiolarien ohne Hartteile gestützt. Ebenso werden unsere Vorstellungen von der Art der Silizifizierung und Schalenbildung auf zwei Möglichkeiten erweitert: (1) die bestehende Auffassung der "simultanen Schalenbildung", derzufolge das gesamte Skelett nahezu gleichzeitig nach mehreren Teilungen der unsilifizierten Zentralkapseln gebildet wird und der (2) "schrittweisen Schalenbildung", bei der aus reifen Zentralkapseln mit Schalen neue durch Teilung hervorgehen. Die Beobachtungen haben interessante Implikationen für die Dynamik von Lebenszyklen bei Radiolarien in heutigen und paläo-ozeanischen Lebensräumen.

 

Italiano

PROVE DI UNA DIVISIONE BINARIA NELLE CAPSULE CENTRALI MATURE DI UN RADIOLARE COLONIALE COLLOSFERIDE: IMPLICAZIONI PER I MODELLI ONTOGENETICI DEL GUSCIO NELLE SPECIE ATTUALI E FOSSILI

In questo lavoro vengono fornite le prove, basate su gusci fossili e specie viventi del radiolare coloniale Acrosphaera, che le capsule centrali mature provviste di guscio possono produrre gusci e capsule centrali figli per mezzo della fissione binaria. Questi dati indicano che, almeno nei radiolari coloniali collosferidi, la riproduzione delle capsule centrali si può verificare dopo la maturazione e può essere responsabile di un rapido incremento della biomassa e delle dimensioni della popolazione in risposta ad ambienti favorevoli. Ciò aumenta la precedente evidenza che le capsule centrali di radiolari coloniali sprovvisti di guscio possano riprodursi per fissione binaria. Inoltre queste osservazioni aumentano la nostra comprensione del modello di silicificazione e formazione del guscio con due possibilità: (1) la visione attuale della "deposizione simultanea del guscio", dove tutti gli scheletri vengono sostanzialmente depositati contemporaneamente a seguito di divisioni multiple delle capsule centrali ascheletriche, e (2) la "deposizione successiva del guscio", dove capsule centrali mature con guscio ne originano altre per mezzo di una fissione binaria ritardata. Queste osservazioni hanno implicazioni interessanti per le dinamiche del ciclo vitale dei radiolari in ambienti attuali e del passato.

Parole Chiave: gusci fossili, radiolare coloniale Acrosphaera, capsule centrali, fissione binaria, radiolari collosferidi, biomassa, dimensioni della popolazione, radiolari coloniali sprovvisti di guscio, silicificazione, ciclo vitale, radiolari, paleoceanico, Quaternario, ecologia, ontogenia del guscio

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