Comparative anatomy of the foramen ovale in the hearts of cetaceans

Abstract

The structure of the cardiac foramen ovale from 17 species representing six cetacean families, the Monodontidae, Phocoenidae, Delphinidae, Ziphiidae, Balaenidae and the Balaenopteridae, was studied using the scanning electron microscope. Eight white whale fetuses (Delphinapterus leucas) and a narwhal fetus (Monodon monoceros) represented the Monodontidae; one fetal and nine neonatal harbour porpoises (Phocoena phocoena) and a finless porpoise fetus (Neophocoena phocoenoides) represented the Phocoenidae; two white-beaked dolphin fetuses (Lagenorhynchus albirostris), four fetal and one neonatal Atlantic white-sided dolphins (Lagenorhynchus acutus), a Risso's dolphin fetus (Grampus griseus), two common bottle-nosed dolphin neonates (Tursiops truncatus), a female short-beaked common dolphin fetus (Delphinus delphis), four killer whale fetuses (Orcinus orca) and two long-finned pilot whale fetuses (Globicephala melas) represented the Delphinidae; two northern bottlenose whale fetuses (Hyperoodon ampullatus) represented the Ziphiidae; one bowhead whale fetus (Balaena mysticetus) represented the Balaenidae and five Common minke whale fetuses (Balaenoptera acutorostrata), one blue whale fetus (Balaenoptera musculus), nine fin whale fetuses (Balaenoptera physalus) and four humpback whale fetuses (Megaptera novaeangliae) represented the Balaenopteridae. The hearts of an additional two incompletely identified toothed and four baleen whale fetuses were also studied. In each species the fold of tissue derived from the cardiac septum primum and subtended by the foramen ovale had the appearance of a short tunnel or sleeve which was fenestrated at its distal end. In the toothed whales the tissue fold was tunnel-shaped with the interatrial septum as the floor whereas in baleen whales it was more sleeve-like. In toothed whales thin threads extended from the fold to insert into the interatrial septum whereas a network of threads covered the distal end of the sleeve in the baleen whales. Similar structures were present in the corresponding cardiac tissues of neonatal Hippopotamidae.

Fig. 1

Schematic diagram of the heart of a cetacean fetus viewed from the left with a window cut into the left atrium. The relative positions of the aorta (A), left common carotid artery (B), ductus arteriosus (DA), pulmonary trunk (P), left atrium (LA), left ventricle (LV), caudal vena cava (CVC), pulmonary vein (PV) and the fold of tissue (F) representing the developed septum primum lying in the lumen of the left atrium are indicated. The latter is distal to the foramen ovale, which it obscures. Pericardial, pleural and lung tissues have been removed.

Fig. 2

(a) Scanning electron micrograph of the foramen ovale (FO) in a white whale (Delphinapterus leucas) fetus viewed from the right atrium, illustrating the curved edge of the crista dividens (CD) of the interatrial septum, and the caudal vena cava (VC). Scale bar = 1 mm. (b) Scanning electron micrograph of the foramen ovale (FO) in a humpback whale (Megaptera novaeangliae) fetus viewed from the right atrium, illustrating the curved edge of the crista dividens (CD) of the interatrial septum and the caudal vena cava (VC). Scale bar = 1 mm.

Fig. 3

(a) Scanning electron micrograph of the fenestrations in the fold of tissue subtended by the foramen ovale of a white whale (Delphinapterus leucas) fetus. Scale bar = 1 mm. (b) Scanning electron micrograph of the left atrium of a harbour porpoise (Phocoena phocoena) fetus illustrating the loose network of threads at the distal end of the tunnel-like fold of tissue subtended by the foramen ovale, and their attachment to the interatrial septum. Scale bar = 1 mm. (c) Scanning electron micrograph of the left atrium of a neonatal harbour porpoise illustrating the apparently coalesced network of threads near the distal end of the tunnel-like fold of tissue subtended by the foramen ovale. Scale bar = 1 mm. (d) Scanning electron micrograph of the distal end of the tunnel-like fold of tissue in a finless porpoise (Neophocoena phocoenoides) fetus illustrating the network of threads and their attachment to the interatrial septum. Scale bar = 1 mm.

Fig. 4

(a) Photograph of the left atrium of an Atlantic white-sided dolphin (Lagenorhynchus acutus) neonate illustrating the network of threads at the distal end of the tunnel-like fold of tissue subtended by the foramen ovale. Scale bar = 1 mm. (b) Scanning electron micrograph of the distal end of the collapsed tube-like fold of tissue in the left atrium of a Risso's dolphin (Grampus griseus) fetus. Blood clots adhere to the flat ribbons of tissue making up the network at its distal end. Scale bar = 1 mm. (c) Scanning electron micrograph of the distal end of the tunnel-like fold of tissue in the heart of a common bottle-nosed dolphin (Tursiops truncatus) neonate. Scale bar = 1 mm. (d) Scanning electron micrograph of the network of threads at the distal end of the tunnel-like fold of tissue subtended by the foramen ovale in a short-beaked common dolphin (Delphinus delphis) fetus. Scale bar = 1 mm.

Fig. 5

(a) Scanning electron micrograph illustrating the network of threads at the distal end of the fenestrated sleeve-like fold of tissue subtended by the foramen ovale in a bowhead whale (Balaena mysticetus) fetus. The sleeve has rolled upon itself. Scale bar = 1 mm. (b) Scanning electron micrograph illustrating the threads at the distal end of the unfenestrated tunnel-like fold of tissue from the foramen ovale in a north atlantic minke whale (Balaenoptera acutorostrata) fetus. Scale bar = 1 mm. (c) Scanning electron micrograph illustrating the network of threads at the distal end of the fenestrated sleeve-like fold of tissue subtended by the foramen ovale in a fin whale (Balaenoptera physalus) fetus. Scale bar = 1 mm. (d) Scanning electron micrograph illustrating the partially autolysed threads at the distal end of the fenestrated sleeve-like fold of tissue subtended by the foramen ovale in a humpback whale (Megaptera novaeangliae) fetus. Scale bar = 1 mm.

Fig. 6

(a) Scanning electron micrograph illustrating the distal end of the fenestrated sleeve-like tissue fold subtended by the foramen ovale in the fetus of an incompletely identified species, possibly sperm whale (Physeter catodon). The tissues labelled AW are sections of atrial wall. Scale bar = 1 mm. (b) Scanning electron micrograph illustrating the network of threads at the distal end of the fenestrated sleeve-like tissue fold subtended by the foramen ovale in an unidentified ‘baleen whale’ fetus. Scale bar = 1 mm.

Fig. 7

(a) The network of threads at the end of the tubular fold of tissue subtended by the foramen ovale of a bowhead whale (Balaena mysticetus) fetus as depicted by Eschricht (1869). (b) The fenestrated thimble-shaped fold of tissue subtended by the foramen ovale of a sei whale (Balaenoptera borealis) fetus as depicted by Schulte (1916). (c) The fenestrations at the distal end of the tubular fold of tissue subtended by the foramen ovale of a fin whale (Balaenoptera physalis) fetus as depicted by Walmsley (1938).

Fig. 8

(a) The fenestrated sleeve-like fold of tissue subtended by the foramen ovale of a hippopotamus (Hippopotamus amphibius) fetus (crown–rump length = 20 cm) illustrating the network of threads at its distal end. Scale bar = 1 mm. (b) The partially autolysed fold of tissue from the foramen ovale of a pigmy hippo (Choeropsis liberiensis) neonate with the branched fibrous subendothelial tissue exposed. The threads at the distal end of the fold of tissue form a loose network. Scale bar = 1 mm.