Secondary circulation in fish: Anatomical organization and physiological significance

Abstract

The secondary circulation is an arterial-capillary-venous system derived from, and in parallel with, the general (primary) circulation of fish. Narrow-bore (2–20 μm diameter × 200–300 μm length), tortuous arterioarterial (interarterial) anastomoses arise from the efferent filamental and efferent branchial arteries of the gill, dorsal aorta, and segmental arteries and condense to form progressively larger secondary arteries. Secondary capillaries have been identified in gills, skin, fins, peritoneal lining, and oral mucosa of bony fish and in gills of many nonteleostean species. Their endothelium is thin-walled with overlapping cell junctions reminiscent of mammalian lymphatic capillaries. Branchial secondary veins drain into primary veins of the head, systemic secondary veins primarily drain into the caudal heart, or into large cutaneous veins, and from there blood enters the primary venous system. Preliminary studies indicate that the secondary circulation is a large-volume (48.4 ml·kg−1, 1.5 times greater than the primary system), low-flow (∼0.3% of cardiac output) network. Microvillous endothelial cells in the primary artery guard the entrance to secondary vessels and restrict access of red blood cells. Close proximity of secondary capillaries to exposed epithelia is suggestive of an ion, volume or immunoregulatory function, although low flow through the secondary system may limit the efficiency of some of these processes. Recent studies indicate that fish lack a true lymphatic system and analogies between the secondary system and lymphatics have been noted. It remains to be determined whether the secondary system is the antecedent of a lymphatic system or a coincidentally similar structure. © 1996 Wiley-Liss, Inc.