Giants in the cold: Morphological evidence for vascular heat retention in the viscera but not the skeletal muscle of the basking shark (Cetorhinus maximus).

Abstract

Fewer than 50 of the over 30,000 extant species of fishes have developed anatomical specializations facilitating endothermy in specific body regions. The plankton-feeding basking shark (Cetorhinus maximus), traditionally classified as an ectotherm, was recently shown to have regionally endothermic traits such as centralized red muscle (RM) along its body trunk and elevated (white) muscle temperatures. However, key anatomical features essential for classification as a regional endotherm, such as the presence of vascular rete mirabile, could not be confirmed in this cold-water giant. This study compared the morphology of heat-generating and heat-retaining tissues - associated with skeletal RM, the cranium and viscera - in the basking shark with those of a confirmed regional endotherm, the porbeagle (Lamna nasus), and a polar ectotherm, the Greenland shark (Somniosus microcephalus). Despite the presence of more medial RM in the basking shark's trunk, the absence of paired lateral vessels and a perfusing rete strongly suggests a lack of RM endothermy in this species. However, the presence of small arterial plexuses in the orbit, along with the discovery of visceral retia associated with the stomach, spleen and valvular intestine, in addition to distinct vascular arrangements in the liver and kidney, indicates potential for cranial and, particularly, visceral endothermy in C. maximus. These specializations, combined with reduced conductive heat loss from partial RM internalization and large body size, may enable C. maximus to maintain regionally elevated body temperatures, facilitating their active lifestyle also in cold-water environments. Enhanced sensory perception and digestive efficiency may aid prey acquisition and processing in the dimly lit meso- and bathypelagic zones, as well as high-latitude regions. Our findings provide initial insights into the thermal adaptations of these circum-globally distributed, highly migratory ram filter feeders. Further research is needed to better understand the eco-physiological implications of these adaptations, especially in the context of rapid ocean warming across their range, including Atlantification in the Arctic, and other anthropogenic pressures in the Anthropocene.