A reappraisal of the respiratory vasculature of the electric eel, Electrophorus sp.

Abstract

The electric eel (Electrophorus sp.) is an air-breathing teleost and has been known as the only fish taxon with direct vascular connections (shunts) between the ventral and dorsal aortas in all four gill arches. The aerial respiratory capillaries of the electric eel have been assumed to be perfused with the pre-branchial blood from these shunt vessels. We re-examined the cardiovascular anatomy and found these prevailing notions to be partly inaccurate. The gills of Electrophorus varii are of the holobranch structure with the afferent (ABA) and efferent (EBA) branchial arteries as discrete anatomical entities in all gill arches. Although the filaments are much shorter than in typical exclusively water-breathing teleosts, normal filamental vasculature intervenes between ABA and EBA in all arches. Yet, there are anastomoses between ABA and EBA, most notably in the fourth gill arch, where the anastomotic vessels have the same diameter as the parent vessels. There are a few, much thinner anastomotic vessels between ABA and EBA and/or the afferent and efferent filamental arteries in the first and second gill arches. The third arch has no anastomoses. The vascular space in the secondary lamellae consists of six to eight parallel interconnected vessels. Capillaries on the dorsal and lateral surfaces of the air-breathing organ are supplied by the branches of the first and second EBAs, while those on the ventral surface receive blood from the hypobranchial arteries, which originate from EBAs in all of the gill arches. Thus, the entire aerial respiratory capillaries are perfused with the post-branchial blood, not with the pre-branchial blood as previously assumed. Oxygenated blood from the air-breathing organ is drained by the anterior cardinal vein on the dorsal and lateral sides and by the inferior jugular vein on the ventral side. The heart shows no anatomical specialization to separate oxygenated and deoxygenated blood, although there is a peculiar rotation such that the bulbus arteriosus and ventricle occur on the right, while the atrium occupies the left side of the pericardial cavity. Thus, the vascular system in the head region of E. varii deviates little from the typical teleostean configuration, except for the proliferation of aerial respiratory capillaries within the air-breathing organ, a considerable degree of gill regression, and anastomoses in gill vessels. These findings, when coupled with the fact that the electric eel obtains 80% of oxygen requirement from air in normoxic water, suggest that heavy reliance on air-breathing is not a driving force for the restructuring of the central cardiovascular system toward double circulation, in which oxygenated and deoxygenated blood is separated.