Edward E. Ruppert

THE FUNCTIONAL ORGANIZATION OF FILTRATION NEPHRIDIA

(1) Based on the classical studies of Goodrich, protonephridia are believed to be phylogenetic antecedents of metanephridia. It is argued here that the primary factor determining the type of nephridium expressed is body size rather than phylogenetic status.

Morphology of metazoan circulatory systems

SummaryThe majority of large, bilaterally-symmetric animals possess two structurally distinct systems of internal fluid transport, the coelomic circulatory system and the blood vascular system (BVS). The coelomic circulatory system is generally situated laterally, lined by a continuous layer of mesodermally-derived cells and moves fluid with cilia or body wall muscles. The BVS occurs in extracellular matrix with the principal vessels situated dorsally and ventrally. The vessels are typically unlined by cells. Fluid is propelled by contraction of overlying muscle cells. Co-occurrence of two systems of internal fluid transport is explained by a segmentation hypothesis: Most large, triploblastic animals are segmented with at least two or three fluid-filled compartments separated by septal bulkheads. Because exchange surfaces (gas, nutrient) are regionally restricted, selective pressure favors a fluid transport system that bridges septal bulkheads. The BVS fulfills this requirement because it is situated in extracellular matrix that is non-cellular and continuous throughout organisms. A survey of animals indicates that all segmented taxa possess a BVS, except Sipuncula, where compensation sacs function as BVS analogues. Loss of the BVS in Hirudinea and other annelids is correlated with the disappearance of septa. Funicular vessels in Bryozoa are compared with BVS in other lophophorates. The fluid transport system of Nemertini and some platyhelminths is shown to conform to the definition of a coelomic circulatory system. This investigation supports Liwanows proposition that the BVS evolved as the progressive modification of extracellular matrix in triploblastic animals. Evolution of coelomic circulatory systems is unresolved.

NEPHRIDIA IN THE LARVAE OF HEMICHORDATES AND ECHINODERMS

The pore canal-hydropore complex in the larvae of echinoderms and hemichordates has long been recognized as an important character establishing a close phylogenetic relationship between the two phyla. An experimental and ultrastructural analysis of this complex in a tornaria and a bipinnaria larva indicates that it is a functional nephridium. The ciliated pore canal drives a constant, unidirectional efflux of coelomic fluid out of the hydropore. Two percent and 14% ofthe body volume are cleared per hour at the hydropore by a tornaria of Schizocardium brasiliense and a bipinnaria of Asterias forbesi, respectively. Fluid recovery by the coelom is from the blastocoel, the presumptive blood vascular space, across basal lamina and podocytes lining the coelomic cavity suggesting that the discharged fluid is formed by ciliary-driven ultrafiltration. Although invertebrate deuterostomes are believed to lack discrete excretory organs, an analysis of the metamorphosis of the larval nephridia suggests that adult echi...

Comparative ultrastructure of the gastrotrich pharynx and the evolution of myoepithelial foreguts in aschelminthes

SummaryStructural and ultrastructural data are presented for the myoepithelial pharynges of 20 species of Gastrotricha representing the marine Macrodasyida and marine and freshwater Chaetonotida. A comparative analysis reveals that pharynges with several plesiomorphic characters occur in Chordodasys among the Macrodasyida and Neodasys among the Chaetonotida. The Gastrotricha are systematized based on pharyngeal characters and the system is shown to be concordant with all recent classifications of the group. The plesiomorphic design of the Gastrotrich pharynx is given as: a cylindrical pharyngeal pump composed of monociliated myoglanduloepithelial cells surrounding a circular or oval lumen; radial myofibrils organized into several cross-striated sarcomeres with Z-discs composed of planar aggregations of dense bodies; excitation-contraction coupling is achieved by peripheral couplings of SR with the sarcolemma; apical cell surface with microvilli protruding through the two-layered cuticle; pharynx with at least 3 longitudinal tracts of monociliated sensory cells; nerves as at least 4 basal intraepithelial, longitudinal tracts of neurites. As a model for muscle cell evolution, the investigation postulates a monociliated, cross-striated myoglanduloepithelial cell as the original muscle cell design within the Gastrotricha. Triradiate myoepithelial foreguts occur only in Bryozoa (Ectoprocta), Gastrotricha, Nematoda and Tardigrada. The potential homology of pharyngeal organization of the latter three phyla is discussed. Based on pharyngeal structure, it is concluded that Gastrotricha (Chaetonotida-Paucitubulatina) and Nematoda share several apomorphic characters and share, therefore, a most recent common ancestor. Affinities of Tardigrada with Aschelminthes are considered feasible but currently inconclusive for lack of sufficient comparative ultrastructural data for the Tardigrada.

Ultrastructure of the Coeloms of Auricularia Larvae (Holothuroidea: Echinodermata): Evidence for the Presence of an Axocoel

A hallmark feature of echinoderm larvae is the development of the left anterior coelom. This coelom, called the axohydrocoel, consists of the morphologically distinct, but undivided, left axocoel and hydrocoel. The axocoelic portion forms a duct that opens to the exterior via a pore on the dorsal surface of the animal. Holothuroid larvae are thought to lack an axocoel, but develop an anterior coelom, duct, and pore that are regarded as parts of the hydrocoel. New ultrastructural data, however, show that holothuroid auricularia larvae possess an axocoel and hydrocoel united together into an axohydrocoel. During development the anterior coelom consists of an interconnected left somatocoel, hydrocoel, and axocoel. The left somatocoel separates from the axohydrocoel and subdivides into left and right somatocoels. The somatocoels and hydrocoel region of the axohydrocoel are lined by a monociliated mesothelium having characteristics of transporting epithelia. The axocoel epithelium, like that of asteroid larvae, is composed of mesothelial podocytes. A duct connects the axocoel directly to the open dorsal pore and is lined with a columnar transporting epithelium. The occurrence of a specialized podocyte-lined cavity between the surface pore and the hydrocoel in echinoderm larvae is indicative of an axocoel. That similar structures occur in auricularia larvae supports the identification of an axocoel in holothuroids.

A deuterostome-like nephridium in the mitraria larva of Owenia fusiformis (Polychaeta, Annelida)

The mitraria larva of 0. fusiformis possesses a pair of nephridi@ which are not typical polychaete larval protonephridia, rather they resemble the pore canal-hydro pore complex ofdeuterostome larvae. An ultrastructural analysis ofthe nephridium reveals a small body cavity, lined by monciciliated podocytes, which opens to the exterior by a monociliated nephridioduct. Extracellular matrix between podocyte pedicels forms the filtration surface and podocyte and nephridioduct cilia produce the pressure gradient driving filtration. Therefore, each nephridium is considered a giant protonephridium. Although this organization is unique to Owenia among the annelids, it is identical ultrastructurally to the hydropore, pore canal, and adjoining coelom ofdeuterostome larvae, which is also a nephndium. It is concluded that this cytological similarity between the nephridia ofthe mitraria and deuterostome larvae reflects a cellular homology which has a wide distribution and is oflimited usefulness in the recognition of relationships. The anatomical differences between them suggest they are, at best, serially homologous organs. Mitraria nephridia compare more favor ably to the typical protonephridia (head kidneys) of polychaete trochophores and larval protonephridia of phoronids. Data support the view that Owenia is primitive among the polychaetes and suggest that the mitraria nephridium represents the plesi omorphic design of protonephridium within the Polychaeta.

Epidermal muscles and peristaltic burrowing in Carinoma tremaphoros (Nemertini): Correlates of effective burrowing without segmentation

SummaryA structural and ultrastructural investigation of epidermis in the esophageal region of Carinoma tremaphoros is correlated with analysis of burrowing locomotion. The pseudostratified epidermis contains multiciliated epidermal cells, gland cells and granule-containing basal or interstitial cells resting on a well-developed basement membrane. Both circular and longitudinal muscles are present within the epidermis, woven between the cells of this layer. These muscles are well-developed along the anterior region of the worm and, like the subepidermal muscles, are a variation of obliquely striated muscle without continuous Z-rods. Epidermal muscles originate as branches from the underlying mesodermal musculature and cross the basement membrane into the epidermis, confirming earlier observations. These muscles are unrelated to myoepithelial epidermal cells described in other metazoans. This condition is considered a secondary derivation consistent with the Gastraea-Enterocoel theory of bilateral metazoan evolution. Carinoma is a peristaltic burrower. Peristaltic waves are limited to the anterior region of the worm where the diameter of the rhynchocoel is maximal and the bilayered epidermal musculature is strongly developed. Following a consideration of burrowing mechanics in annelids, supernumerary epidermal muscles in Carinoma are interpreted as prerequisites to peristaltic burrowing effectiveness in a non-segmented coelomate.

The size range of suspended particles trapped and ingested by the filter-feeding lancelet Branchiostoma floridae (Cephalochordata: Acrania)

Lancelets of the genus Branchiostoma (amphioxus) are widespread and locally abundant filter-feeding animals in shallow coastal waters of the south-eastern US (up to 5000 ind/m 2 ) and in temperate and tropical seas worldwide (up to 9000 ind/m 2 ). Lancelets are consumed by bottom-dwelling fish and humans. As part of a larger project to aquaculture lancelets, an experiment was conducted to determine the range of diameters of suspended particles filtered and ingested by the Florida lancelet, Branchiostoma floridae (Chordata: Cephalochordata). After a period of starvation, animals were exposed to a suspension of tracer particles of seven different diameters (range 90–0.062 μm) and the protein, ferritin (0.012 μm) and their faeces were examined subsequently for the presence or absence of tracer. Particles ranging from 90–0.062 μm, but not ferritin, were filtered and ingested. Many of the 90 μm diameter particles, however, were excluded from entering the body by the oral cirri. Under experimental conditions, B. floridae filters and ingests particles in the range of ∼100–0.062 μm (microplankton to colloidal particles). This result suggests that the lancelet diet, like that of appendicularians, includes microbial as well as phytoplankton production.

Primordial Germ Cells of Synaptula hydriformis (Holothuroidea; Echinodermata) Are Epithelial Flagellated-Collar Cells: Their Apical-Basal Polarity Becomes Primary Egg Polarity

The primordial germ cells (PGCs) of a recently metamorphosed juvenile Synaptula hydriformis occur with somatic cells in the germinal epithelium of the gonad. As part of the epithelium, PGCs rest on a basal lamina, extend apically towards a lumen, are joined to other cells of the epithelium via apicolateral junctions, and express apical-basal polarity. Each PGC has an apical flagellum that is surrounded by a collar of microvilli. The apicolateral junctions of PGCs consist of apical adhering and subapical septate junctions. Hemidesmosomes attach the PGCs to the basal lamina. Although the somatic cells form an incomplete layer over the PGCs, both the PGCs and somatic cells remain exposed to the apical lumen and retain contact with the basal lamina. The peritoneum is the outermost layer of the gonad and faces the perivisceral coelom. The epithelial-cell characteristics expressed by cells of the peritoneum are identical to those of the germinal epithelium. PGCs of S. hydriformis are epithelial flagellated-collar cells and express the apical-basal polarity that is typical of epithelial cells. The apical-basal polarity of the oocyte, animal-vegetal axis of full-grown eggs, and anterior-posterior axis of larvae and adults are all in correspondence. Thus the polarity of the germinal epithelium may determine the primary body axis of the next generation.

Primordial germ cells and oocytes of Branchiostoma virginiae (Cephalochordata, Acrania) are flagellated epithelial cells: relationship between epithelial and primary egg polarity

Primordial germ cells (PGCs) are described from the gonad of c. 2 cm juvenile Branchiostoma virginiae; early oocytes (c. 10 microm) and enlarging, previtellogenic oocytes (c. 35 microm) are described from the ovary of c. 5 cm adults. The germinal epithelium of the juvenile gonad and adult ovary is composed of both germinal and somatic cells. In the juvenile, somatic cells retain contact with the basal lamina of the germinal epithelium though their perikarya may be displaced towards the lumen; the germinal epithelium is, therefore, a simple but pseudostratified epithelium. In the adult ovary, somatic cells may lose contact with the basal lamina and the epithelium appears to become stratified. PGCs and oocytes are identified as germ cells by the presence of nuage. PGCs and oocytes are polarised epithelial cells. They rest on a basal lamina, extend apically towards a lumen, form adhering junctions with neighbouring cells, and exhibit apical-basal polarity. PGCs and early oocytes have an apical flagellum with an associated basal body, accessory centriole, and one or more striated rootlet fibres. The flagellum is surrounded by a collar of microvilli. Once oocytes begin to enlarge and bulge basally into the connective tissue layer, the flagellum is lost, but the basal bodies and ciliary rootlets are present at the apex of 35 microm oocytes. Similarities of the oogenic pattern in cephalochordates and echinoderms indicate that the establishment of egg polarity in deuterostomes is influenced by the polarity of the germinal epithelium.