Permeability of external gill filaments in the embryonic shark. Electron microscopic observations using horseradish peroxidase as a macromolecular tracer.

External gill filaments of sharks are purely transient embryonic structures. They contain a single vascular sinusoidal loop that is continuous with the afferent and efferent branchial arteries. Each filament is comprised of a squamous epithelial bilayer that rests upon a prominent basal lamina. A collagenous stroma separates the epithelium from the underlying endothelium. The epithelium, from an embryo 4.5 cm in total length, is characterized by microvilli with smooth walled vesicles at their bases, a luminal glycocalyx, prominent tubular and vesicular elements, rough endoplasmic reticulum, a Golgi complex, a flattened nucleus, coated vesicles, lipid-like inclusion bodies and sparse cytoplasmic fibrils. Adjacent epithelial cells are joined by a zonula occludens, a zonula adherens and up to five maculae adherentes. The endothelium possesses mitochondria, rough endoplasmic reticulum, a Golgi complex, coated vesicles and many micropinocytotic vesicles on both the adluminal and abluminal surfaces. The endothelium has no basal lamina and is not associated with smooth muscle. After exposure to horseradish peroxidase (HRP) for 10 min, reaction product nearly occludes the cytoplasm of some surface epithelial cells. The deeper epithelial cells have reaction product in smooth walled vesicular and tubular elements. Reaction product is also present in smooth walled endothelial vesicles. Gill filaments from a 10 cm embryo show marked changes from earlier stages. In the epithelial cells, there is an increase in the number of cytoplasmic filaments and the formation of a dense terminal web. Fewer vesicles, tubules, rough endoplasmic reticulum and mitochondria, and a less elaborate Golgi complex characterize the epithelium. The endothelium remains unchanged. The amount of collagen increases and fibroblasts are observed in the stroma. These modifications contribute to the strength of the filaments and allow the gills to withstand increased abrasion by the developing skin denticles. These experiments establish the capability of external gill filaments to take up a macromolecular tracer in the form of horseradish peroxidase. Later in development, the yolk sac of R. terraenovae becomes modified as a yolk sac placenta which functions both in respiration and hematrophic nutrition. In viviparous sharks, the uterus elaborates nutrient-rich secretions. External gill filaments may thus serve as a nutrient absorptive membrane before the establishment of the yolk sac placenta as well as perform its respiratory function.