Orbital rete and red muscle vein anatomy indicate a high degree of endothermy in the brain and eye of the salmon shark

Abstract

Tubbesing, V. A and Block, B. A. 2000. Orbital rete and red muscle vein anatomy indicate a high degree of endothermy in the brain and eye of the salmon shark. Ð Acta Zoologica (Stockholm) 81: 49±56The salmon shark has been ranked as the most endothermic lamnid shark based upon geographical range, extent of slow twitch muscle, supra-hepatic rete size, and limited temperature measurements, yet its anatomy has remained largely undescribed, and measurements of brain or eye temperatures have not been reported. In this study, four specimens are examined to determine if the morphological requirements for warming the brain and eyes are present. A well-developed arterial orbital rete lies within a venous sinus on both sides of the cranium. Cool, oxygenated blood from the gills can pass through the vessels of this exchanger before reaching the brain or eyes. Since venous blood in the sinus flows opposite the arterial blood, counter-current heat exchange can occur. A vein originating in the red swimming muscle likely contributes to the warmth of the venous sinus by supplying blood directly from the warmest region of the shark. Before collecting in the orbital sinus, this red muscle vein bathes the brain in warm blood. These morphological data suggest the salmon shark has a significant capacity to warm the brain and eyes.

Seasonal foraging movements and migratory patterns of female Lamna ditropis tagged in Prince William Sound, Alaska

“…Pacific salmon and Pacific herring aggregations in the Gulf of Alaska) from optimal thermal habitat (warmer temperatures at lower latitudes). The physiological adaptation of endothermy (Tubbesing & Block, 2000; Anderson & Goldman, 2001) probably underlies L. ditropis choosing habitat with a consistent source of concentrated prey over the energetic demands of remaining in cold waters into winter months in the Gulf of Alaska. The energetic advantages of remaining in the northern Gulf of Alaska, however, may diminish as spatio‐temporal declines in prey density and surface water temperatures occur into autumn and winter months.…”

“…Salmon sharks belong to the family Lamnidae, together with four other species: the white shark Carcharodon carcharias (L.), the shortfin mako Isurus oxyrinchus Rafinesque, the longfin mako Isurus paucus Guitart Manday and the porbeagle Lamna nasus (Bonnaterre). The capacity to elevate body temperature (endothermy) has been documented for all lamnids (Lowe & Goldman, 2001) and salmon sharks are ranked as the most endothermic in this family (Tubbesing & Block, 2000). Whether L. ditropis is able to maintain high and uniform temperature values regardless of changes in ambient temperature (the homeothermy hypothesis of Lowe & Goldman, 2001), however, requires further investigation.…”

Circulating serotonin in vertebrates

“…Thermoregulation in tuna was previously suggested to be based on changes in retial blood flow [57]. Retia are nets of blood vessels that can retain heat with exceptional efficiency [58]. How the absence of vasoactive circulating serotonin might support this view requires further investigation.…”

Evidence for cranial endothermy in the opah (Lampris guttatus)

“…In the other tuna species, there is no evidence of modified extraocular muscle (Block et al, 1982;Block, 1990;Sepulveda et al, 2007), and contraction of the extraocular muscles (Block and Finnerty, 1994) or active metabolism within the brain (Block, 1987b;Block et al, 1982) have been proposed as possible sources of heat for cranial endothermy in those species. In lamnid sharks, heat produced within the slow-oxidative myotomal muscle is transferred to the cranial area via the unique red muscle vein and the myelonal vein (Block and Carey, 1985;Carey et al, 1985;Wolf et al, 1988;Alexander, 1998;Tubbesing and Block, 2000). In addition, contraction of extraocular muscles may also contribute to heat production in these sharks (Wolf et al, 1988;Alexander, 1998).…”

“…The lamnid sharks have paired orbital retia, each made of an arterial plexus branching from the highly coiled pseudobranchial and efferent hyoidean arteries surrounded by warm blood within the orbital venous sinus (Block and Carey, 1985;Carey et al, 1985;Alexander, 1998;Tubbesing and Block, 2000). The red muscle vein supplies warm blood to the orbital sinus via the myelonal vein (Wolf et al, 1988;Tubbesing and Block, 2000).…”