Erect tube growth in Rhabdopleura compacta (Hemichordata: Pterobranchia) from off Start Point, Devon

Patterns of tube construction in the upright tubes of Rhabdopleura compacta are described. Tube building is seen to be a highly regular process, with growth extending over more than one season. Participation in the building of any one tube can involve multiple generations of zooids. Spatial awareness in a zooid adding new material to a pre-existing tube can be demonstrated. This shows that the construction of the tube is strictly determined, either by environmental or genetic mechanisms, rather than being a function of developing zooid morphology, as previously suggested, or random processes.     

Decay and composition of the hemichordate Rhabdopleura: implications for the taphonomy of graptolites

Although the graptolites lacked biomineralised tissue, their skeletons are abundantly preserved in deeper-water mudstones. Decay experiments and observations on the closely related living hemichordate Rhabdopleura demonstrate that the periderm and stolon are highly resistant to decay, remaining intact for months, whereas the zooids are unrecognizable within days. The extreme rarity of the preservation of traces of the zooids in graptoloids reflects their planktic lifestyle; the zooids had normally decayed before burial. Curie-point-gas-chromatography (Py-GC) and Curie-point-gas-chromatography-mass spectrometry (Py-GC-MS) of the periderm of Rhabdopleura confirms that proteinaceous organic matter is a major constituent. Ultrastructurally preserved graptolite periderm (Ordovician, Oklahoma; Silurian, Arctic Canada), on the other hand, is a highly altered kerogen-like substance rich in aliphatic biomacromolecules. The composition of the preserved graptolite periderm reflects diagenetic replacement by components probably mainly derived from algal cell walls.     

Preservation of soft tissues in Silurian graptolites from Latvia

The contractile stalks of graptoloid zooids are preserved as organic carbon residues in thecae of the middle Llandovery graptoloid graptolites Rastrites geinitzii and Neolagarograptus? sp. from the Aizpute‐41 core, Latvia. The contractile stalks are surrounded by equant pyrite crystals, resulting in three‐dimensional preservation of the graptolite rhabdosomes, and are associated with sediment of similar composition to, and derived from, the adjacent matrix. Matrix entered the thecae after pyrite crystal growth and filled some of the space left by collapse of the contractile stalks and some intercrystalline cavities; other space is partially infilled by diagenetic minerals. The contractile stalks are parallel‐sided and occupy up to one‐half the metathecal width, which is not inconsistent, assuming post‐mortem shrinkage, with the suggestion that graptoloid zooids filled their thecal tubes in life. The location of the preserved soft tissues, towards the distal ends of the metathecae, is very different from that predicted by decay experiments on the extant pterobranch hemichordate Rhabdopleura; the latter's soft tissues may thus not be a reliable analogue for those of these Silurian graptoloids.     

The prosicular stage of Rhabdopleura (Pterobranchia: Hemichordata)

After settling, the larva of Rhabdopleura surrounds itself with a collagenous dome. Later, the zooid breaks through the wall of the dome and builds the horizontal tube part of the coenecium on to the dome.
The dome is a layered structure, unknown in other parts of the coenecium. whereas the horizontal tube is made up of rings in the classical manner of the adult coenecium. The construction of these two parts is different. The techniques used to reinforce the horizontal tube show a marked similarity to the cortical bandages recently described in the fossil graptolites, and give support to the claim that they are ancestral to Rhabdopleura. There are two sorts of early horizontal tube, one is a straight tube, and the other is longer and coiled. The hole in the dome through which the zooid emerges to build the horizontal tube is probably produced by a chemical boring of the zooid, and supports the hypothesis that the zooids can bore holes in shells and corals.     

An intertidal Rhabdopleura (Hemichordata, Pterobranchia) from Fiji

Rhabdopleura has been discovered living in coral rubble on reefs in Fiji. The habitat is unusual, being the underside of coral boulders in the intertidal zone. Some features of the environment and the fauna associated with the Rhabdopleura are briefly described. The Rhabdopleura zooids exhibit other modes of tube building besides the regular cylindrical horizontal and erect tubes. The colony ramifies through interstices in the dead coral and the zooids can line larger cavities within the coral with coenecial tissue. It is probably these cavities, together with the overall porosity of coral, that retain enough water to keep the zooids alive while the intertidal reef flat is exposed to the air. Within the depths of the coral the black stolons are frequently naked. The species is probably R. normani Allman.     

Fossilization processes of graptolites: insights from the experimental decay of Rhabdopleura sp. (Pterobranchia)

Laboratory experiments documenting the decomposition pattern of extant organisms are used to reconstruct the anatomy and taphonomy of fossil taxa. The subclass Graptolithina (Hemichordata: Pterobranchia) is a significant fossil taxon of the Palaeozoic era, represented by just one modern genus, Rhabdopleura. The rich graptolite fossil record is characterized by an almost total absence of fossil zooids. Here we investigated the temporal decay pattern of Rhabdopleura sp. tubes, stolons and single zooids removed from the tubarium. Tubes showed decay after four days, when fuselli began to separate from the tube walls. This rapid loss may explain the absence of fuselli from some graptolite fossils. The black stolon did not show decay until day 155. One day after their removal, zooids quickly decomposed in the following temporal sequence: (1) tentacles; (2) ectoderm; (3) arms; (4) gut; (5) cephalic shield, leading to complete disappearance of recognizable body parts in the majority of experimental zooids within 64–104 h. The most resistant zooid features to decay (61 days) were black‐pigmented granules. These results indicate that tubes and the black stolon would persist for weeks across death, transport and burial, whereas a complete decay of zooid features occurs in few days, providing an explanation for the overall poor record of fossil graptolite zooids and suggesting that recorded silhouettes of fossil zooids may be attributed to fossil decay‐resistant pigments.     

Multizooidal Budding in Parasmittina trispinosa (Johnston) (Bryozoa,Cheilostomata)

Two principally different wall types occur in the bryozoan colony: Exterior walls delimiting the super-individual, the colony, against its surroundings and interior walls dividing the body cavity of the colony thus defined into units which develop into sub-individuals, the zooids. In the gymnolaemate bryozoans generally, whether uniserial or multiserial, the longitudinal zooid walls are exterior, the transverse (proximal and distal) zooid walls interior ones. The radiating zooid rows grow apically to form “tubes” each surrounded by exterior walls but subdivided by interior (transverse) walls. The stenolaemate bryozoans show a contrasting mode of growth in which the colony swells in the distal direction to form one confluent cavity surrounded by an exterior wall but internally subdivided into zooids by interior walls. In the otherwise typical gymnolaemate Parasmittina trispinosa the growing edge is composed of a series of “giant buds” each surrounded by exterior walls on its lateral, frontal, basal and distal sides and forming an undifferentiated chamber usually 2–3 times as broad and 3 or more times as long as the final zooid. Its lumen is subdivided by interior walls into zooids 2–3, occasionally 4, in breadth. This type of zooid formation is therefore similar to the “common bud” or, better-named, “multizooidal budding” characteristic of the stenoleamates but has certainly evolved independently as a special modification of the usual gymnolaemate budding.     

Cell proliferation and growth inZoothamnium niveum (Oligohymenophora, Peritrichida) — Thiotrophic bacteria symbiosis

Chemolithoautotrophic, sulphide-oxidizing (thiotrophic) symbioses represent spectacular adaptations to fluctuating environmental gradients and survival is often accomplished when growth is fuelled by sufficient nourishment through the symbionts leading to fast cell proliferation. Here we show 5′-bromo-2′ deoxyuridine (BrdU) pulse labelling of vegetative growingZoothamnium niveum, a colonial ciliate obligately associated with thiotrophic ectosymbionts, and demonstrate age related growth profiles in three heteromorphic host cell types. At the colony’s apex, a large top terminal zooid performed high proliferation activity, which decreased significantly with increasing colony age but was still present in old colonies indicating that this cell possesses lifelong cell division potential. In contrast, terminal branch zooids proliferated independent of colony age but appeared to be limited by their cell division capacity predetermined by branch size, thus leading to the strict, feather-shaped colony form. Appearance of labelled terminal branch zooids allowed us to distinguish a highly proliferating apical colony region from an almost inactive, senescent basal region. In macrozooids attached to the colony, extensive BrdU labelling suggests that DNA synthesis occurs in preparation for a new generation. As motile swarmers, the macrozooids seem to be arrested in the cell cycle and mitosis and cell division occur when the swarmer settles and transforms into a top terminal zooid buildingup a new colony.     

Cyclical generation and degeneration of organs in a colonial urochordate involves crosstalk between old and new: a model for development and regeneration

Botryllus schlosseri is a colonial marine urochordate in which all adult organisms (called zooids) in a colony die synchronously by apoptosis (programmed cell death) in cyclical fashion. During this death phase called takeover, cell corpses within the dying organism are engulfed by circulating phagocytic cells. The "old" zooids and their organs are resorbed within 24-36 h (programmed cell removal). This process coincides temporally with the growth of asexually derived primary buds, that harbor a small number of undifferentiated cells, into mature zooids containing functional organs and tissues with the same body plan as adult zooids from which they budded. Within these colonies, all zooids share a ramifying network of extracorporeal blood vessels embedded in a gelatinous tunic. The underlying mechanisms regulating programmed cell death and programmed cell removal in this organism are unknown. In this study, we extirpated buds or zooids from B. schlosseri colonies in order to investigate the interplay that exists between buds, zooids, and the vascular system during takeover. Our findings indicate that, in the complete absence of buds (budectomy), organs from adult zooids underwent programmed cell death but were markedly impaired in their ability to be resorbed despite engulfment of zooid-derived cell corpses by phagocytes. However, when buds were removed from only half of the flower-shaped systems of zooids in a colony (hemibudectomy), the budectomized zooids were completely resorbed within 36-48 h following onset of programmed cell death. Furthermore, if hemibudectomies were carried out by using small colonies, leaving only a single functional bud, zooids from the old generation were also resorbed, albeit delayed to 48-60 h following onset of programmed cell death. This bud eventually reached functional maturity, but grew significantly larger in size than any control zooid, and exhibited hyperplasia. This finding strongly suggested that components of the dying zooid viscera could be reutilized by the developing buds, possibly as part of a colony-wide recycling mechanism. In order to test this hypothesis, zooids were surgically removed (zooidectomy) at the onset of takeover, and bud growth was quantitatively determined. In these zooidectomized colonies, bud growth was severely curtailed. In most solitary, long-lived animals, organs and tissues are maintained by processes of continual death and removal of aging cells counterbalanced by regeneration with stem and progenitor cells. In the colonial tunicate B. schlosseri, the same kinds of processes ensure the longevity of the colony (an animal) by cycles of death and regeneration of its constituent zooids (also animals).     

Developmental pattern of colonies in the polystyelid ascidian,Polyandrocarpa misakiensis

Summary

The growth pattern of zooids formed asexually by budding was studied in the colonial ascidian, Polyandrocarpa misakiensis. Each colony started from a blas- tozooid (the first generation) on the glass plate in two series of experiments. To evaluate the growth of colonies, lineage of all the zooids of three successive generations was traced on photographs which were taken once a week. The zooids of the first generation produced many buds from any basal margin of the zooidal body, and those of the second generation produced a small number of buds mainly from anterior parts of the zooidal body. The zooids of the second generation produced by early budding of mother zooids were clearly more prolific than those produced by late budding. Circular colonies which developed around a zooid of the first generation consisted of stratified zones of successive generations. Each zone was composed of two subzones; the outer one mainly containing early-produced zooids, and the inner one mainly containing late-produced zooids. The zooids in the marginal area of colony are early-produced ones from generation to generation. The seawater temperature may influence the growth of zooids and/or the frequency of budding.     

Quantitative observations on asexual reproduction of Aeolosoma viride (Annelida,Aphanoneura)

Agametic reproductive activity (via paratomy) of Aeolosoma viride was analyzed throughout the life cycle in individually reared specimens. Aeolosoma viride is organized in linear chains of 3–4 zooids; the main zooid is anterior, and the secondary zooids are positioned posterior to the main zooid in inverse order with respect to their degree of growth, the most advanced being at the posterior end, and those less advanced nearer the main zooid. On average, worms lived 66±10 d and produced 57±6 offspring. A budding area located in the sub‐terminal part of the main zooid produced chaetigers that formed the origin of the secondary zooids. A growth zone was located in the posterior end of each secondary zooids. Fission occurred between the penultimate and the last zooid of the chain. Just before fission, the growth zone of each secondary zooid became a budding area. Agametic reproduction was via multiple paratomy with linear succession of the secondary zooid and terminal fission. The structure of the chain was therefore modulated by the interaction of the processes of budding, growth, cephalic differentiation, and fission, which occurred continuously and on different timescales. Values of parameters describing paratomic activity (interval between origin of the zooids, time to produce a chaetiger, growth time of the zooids, and interval between the fission of the filial chains) are low early in an individual's life, but increase during senescence. Due to its relatively rapid lifecycle and high reproductive activity, A. viride is a convenient experimental organism for the study of agametic reproduction.     

Unconventional signalling in tunicates

The zooids in colonial tunicates do not appear to be directly interconnected by nerves, but this has not prevented the evolution of coordinated behaviour in several groups. In Botryllus and other colonial styelid asci‐dians the endothelium lining the blood vessels is excitable and transmits action potentials from cell to cell via gap junctions. These signals mediate protective contractions of the zooids and synchronize contractions of the vascular ampullae. In didemnid ascidians such as Diplosoma a network of myocytes in the tunic serves to transmit excitation and to cause contractions of the cloacal apertures. Individual zooids of Pyrosoma protect themselves by closing their siphons and arresting their branchial cilia when stimulated. At the same time a flash of light is emitted. Neighbouring zooids sense the flash with their photoreceptors and respond in turn with protective responses and light emission. Protective responses thus spread by photic signalling and propagate from zooid to zooid through the colony in a saltatory manner. In chains of Salpafusifortnis, changes in the direction and/or speed of swimming are transmitted from zooid to zooid via adhesion plaques. When a zooid is stimulated, its body‐wall epithelium conducts action potentials to the plaque connecting it to the next zooid, exciting receptor neurons in that zooid. These receptors have sensory processes that bridge the gap between the two zooids. The sensory neurons so excited in the second zooid conduct impulses to the brain where they alter the motor output pattern, and at the same time generate epithelial action potentials that travel to the next zooid in line, where the same thing happens.

It is not clear why these unconventional signalling methods have evolved but the tunic may be an inhospitable environment for nerves, making conventional nervous links impossible.     

Does polymorphism predict physiological connectedness? A test using two encrusting bryozoans

A colonial lifestyle necessitates communication between colony members to coordinate functions and enable resource sharing through physiological integration. Colonial integration is predicted to increase with both the size of the colony and the level of specialization (polymorphism). In modular colonies, although integration might be reflected in structural characteristics such as module spacing or branching patterns, physiological integration is fundamentally dependent on the level of connectedness between modules. In cheilostome bryozoans, funicular tissue links adjacent zooids through pores within zooid walls and is the most likely means of nutrient transport within colonies. We sought to determine whether the relative numbers of pores (septulae) and pore plates (septal chambers) per zooid differed across colony regions in a monomorphic species, Watersipora subtorquata, and one showing some polymorphism, Mucropetraliella ellerii. Within each species, the morphology of pore plates corresponded to functional predictions based on their position within the zooid, and connection numbers per zooid increased with colony size. Contrary to expectations, however, the more complex species, M. ellerii, had significantly fewer porous connections per zooid than W. subtorquata. Physiological connectedness was therefore not predicted by simple assessment of polymorphism in these species and may not be sufficient to infer colonial integration in related taxa.     

Some regularities in the development of encrusting colonies of Cribrilina annulata (Fabricius, 1780)

The growth of encrusting colonies was studied with mathematical model. It was shown that encrusting growth takes place under increasing competition for the substrate inside the colony. The model was tested on the example of Cribrilina annulata collected in White Sea on Laminaria saccarina. All colonies were mapped, zooids were measured and genealogical connections between them were established. A number of gradients were revealed by statistical methods. The intensity of budding decreases in astogeny according to theoretical predictions. It was shown that development of Cribrilina annulata colonies is strictly determined by gradients that can be caused by shortage of substrate space. It leads to the suppression of budding and changing in zooid size. Increasing substrate shortage is predictable and caused by the regularities in of zooid budding. The growth of colony stops after exhausting of potentially available substrate.     

The dormant buds of Rhabdopleura compacta (Hemichordata)

Rhabdopleura has an overwintering stage that consists of two layers of cells surrounding a central yolk mass. This cellular part is surrounded by a thick electron dense capsule which is secreted by the bud itself. The capsule is probably impervious and protective to its contents. Blood vessels join the buds to the zooids of the colony. They form the probable route of transfer of yolk from the zooids to the dormant bud. The capsule of the dormant bud has some structural features in common with the black stolon of the adult zooids. The black stolon is probably formed in a manner similar to that which made the fusellar fabric of the periderm of fossil graptolities.     

A morphological study of nonrandom senescence in a colonial urochordate

Botryllus schlosseri is a clonally modular ascidian, in which individuals (zooids) have a finite life span that is intimately associated with a weekly budding process called blastogenesis. Every blastogenic cycle concludes with a synchronized phase of regression called takeover, during which all zooids in a colony die, primarily by apoptosis, and are replaced by a new generation of asexually derived zooids. We have previously documented that, in addition to this cyclical death phase, entire colonies undergo senescence during which all asexually derived individuals in a colony, buds and zooids, die in concert. In addition, when a specific parent colony (genet) is experimentally separated into a number of clonal replicates (ramets), ramets frequently undergo senescence simultaneously, indicating that mortality can manifest itself in nonrandom fashion. Here, we document a morphological portrait of senescence in laboratory-maintained colonies from Monterey Bay, California, that exhibit nonrandom mortality. Nonrandom senescence proceeded according to a series of characteristic changes within the colony over a period of about one week. These changes included systemic constriction and congestion of the vasculature accompanied by massive accumulation of pigment cells in the zooid body wall (mantle), blood vessels, and ampullae; gradual shrinkage of individual zooids; loss of colonial architecture, and ultimately death. At the ultrastructural level, individual cells exhibited changes typical of ischemic cell death, culminating in necrotic cell lysis rather than apoptosis. Collectively, these observations indicate that senescence is accompanied by unique morphological changes that occur systemically, and which are distinct from those occurring during takeover. We discuss our findings in relation to current experimental models of aging and the possible role of a humoral factor in bringing about the onset of senescence.     

Suppression of programmed cell death regulates the cyclical degeneration of organs in a colonial urochordate

The survival of animal tissues and organs is controlled through both activation and suppression of programmed cell death. In the colonial urochordate Botryllus schlosseri, the entire parental generation of zooids in a colony synchronously dies every week as the asexually derived generation of buds reaches functional maturity. This process, called takeover, involves massive programmed cell death (PCD) of zooid organs via apoptosis followed by programmed removal of cell corpses by blood phagocytes within approximately 1 day. We have previously reported that developing buds in conjunction with circulating phagocytes are key effectors of zooid resorption and macromolecular recycling during takeover, and as such engineer the reconstitution of a functional asexual generation every week [Lauzon, R.J., Ishizuka, K.J., Weissman, I.L., 2002. Cyclical generation and degeneration of organs in a colonial urochordate involves crosstalk between old and new: a model for development and regeneration. Dev. Biol. 249, 333-348]. Here, we demonstrate that zooid lifespan during cyclic blastogenesis is regulated by two independent signals: a bud-independent signal that activates zooid PCD and a bud-dependent, survival signal that acts in short-range fashion via the colonial vasculature. As zooids represent a transient, mass-produced commodity during Botryllus asexual development, PCD regulation in this animal via both activation and suppression enables it to remove and recycle its constituent zooids earlier when intra-colony resources are low, while maintaining the functional filter-feeding state when resources are adequate. We propose that this crosstalk mechanism between bud and parent optimizes survival of a B. schlosseri colony with each round of cyclic blastogenesis.     

Phenotypic plasticity of reproductive effort in a colonial ascidian,Botryllus schlosseri

Phenotypic plasticity is the capability of a genotype to produce different phenotypes in different environments. Previous studies have indicated phenotypic variability in asexual, male, and female reproduction in Botryllus schlosseri, a hermaphroditic, colonial ascidian, but not explicitly tested for genotype by environment interactions that indicate genetic variation in plastic responses. Consequently, clones derived from an estuarine population were deployed at their native site and a warmer, higher productivity site 10 km up-river. Male reproduction was assayed by testis size, female reproduction by the number of eggs produced, and asexual reproduction by colony growth rate. To test for ontogenetic effects, data were collected from two different generations of zooids born in the field. Analyses of variance indicated plasticity in asexual and female reproduction during the first zooid generation and plasticity in all three traits during the third zooid generation. Reaction norms varied significantly among genotypes in direction and magnitude for asexual reproduction at both times, implying that selection on asexual reproduction is weak. Sperm production during the third zooid generation was significantly lower at the nonnative site, but there was no genotype by environment interaction. The reaction norms for female reproduction varied significantly among genotypes in direction and magnitude during the first zooid generation, but only varied in magnitude during the third generation, with egg production being higher in all genotypes at the nonnative site. Comparisons of weighted frequency distributions between sites demonstrated that differences in egg production in the third generation were due to increases in the proportion of reproductive zooids within a colony. The greater emphasis on female reproduction at a site associated with higher food availability and temperature, and the greater emphasis on male reproduction at a colder, food-limited site, supports predictions from sex allocation theory.     

ISOLATED GRAPTOLITES FROM THE LITUIGRAPTUS CONVOLUTUS BIOZONE (SILURIAN, LLANDOVERY) OF DALARNA, SWEDEN

Abstract:  Isolated material of 13 graptolite species from the Aeronian (middle Llandovery) Lituigraptus convolutus Biozone is described. A considerable amount of late astogenetic peridermal thickening is revealed in Normalograptus scalaris and Rivagraptus bellulus . As a result, in the former, thecal morphology is modified from climacograptid to pseudoglyptograptid; in both species, the virgella becomes robust. In Metaclimacograptus minimus and Me. sp., it is shown that the dorsal metathecal wall forms the genicular hood, whereas in N. nikolayevi , the infragenicular wall of the succeeding theca forms the distal thecal apertural margin. Pribylograptus argutus exhibits typical pribylograptid thecae along the length of the available rhabdosome fragments. Characters differentiating Campograptus lobiferus from C. harpago include the greater dorso-ventral width and more rapid increase in dorso-ventral width of the former and the greater recurving of distal thecae and presence of thecal spines/processes on all thecae of the latter. Lituigraptus convolutus has rastritiform thecae proximally; thecal apertures throughout the rhabdosome are crescentic and laterally expanded.     

Graptoloid feeding efficiency, rotation and astogeny

Two methods are used to examine feeding strategies in graploloids; the first profiles different sets of zooids on the colony, the second treats the colony as a whole. Both of these techniques have advantages. The choice between them brings into question our concepts of the degree of coloniality shown by graptoloids. Using a whole colony model. graptoloids can be shown to have sampled the water with variable efficiency. as defined in this paper. Planar forms were relatively inefficient, generally sampling less than 10% of the available water. Inclined forms frequently approached 75% efficiency. Biserial forms and strdight monograptids roulinely exceeded 100%. sampling each unit of water more than once. Rotation of the rhabdosome during movement increased the efficiency of horizontal and inclined forms. It reduced the efficiency of scandent biserials and straight monograptids. These were both advantageous effects. Astogenetic changes in colony size and form would have had a profound effect on feeding efficiency.□ Graptoloid, ecology, astogeny