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Cranial endothermy and a putative brain heater in the most basal tuna species, Allothunnus fallai

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Abstract:

Field studies on the slender tuna Allothunnus fallai revealed cranial temperatures that were 4·8 ± 0·4° C (mean ±s.d.) above the ambient sea surface temperature. Dissections aimed at documenting the cranial heat source revealed a fused extraocular muscle complex positioned beneath the brain of this basal tuna species. The muscle complex is structurally distinct from that documented for any other fish species. In A. fallai, all four extraocular rectus muscle pairs (superior, inferior, medial and lateral rectus) are incorporated into one distinct tissue complex which is positioned between the orbits and in direct contact with the braincase. A combination of morphological, physiological and biochemical techniques were used to characterize the modified muscle tissue, and high-resolution magnetic resonance imaging was used to illustrate its association with the brain and optic nerves. The modified eye muscles lack organized contractile proteins and are perfused by an extensive vascular counter-current system that originates from the internal carotid artery. Vessel diameters, artery–vein configuration, and anatomic position between the systemic circulation and the warm eye muscles all suggest that this system is a heat exchanger. Collectively, these findings suggest that A. fallai has evolved extraocular muscles that may function to warm the brain and eye region. This is the first record of a cranial modification comprised of all four rectus muscles and the only documented occurrence of this mechanism for cranial endothermy among the tunas.

Keywords: Allothunnus; Scombridae; endothermy; heater tissue; temperature; tuna

Document Type: Regular Paper

DOI: https://doi.org/10.1111/j.1095-8649.2007.01446.x

Affiliations: 1: Department of Biological Science, California State University Fullerton, Fullerton, CA 92834, U.S.A. 2: Center for Functional Magnetic Resonance Imaging, University of California, San Diego, La Jolla, CA 92093-0677, U.S.A. 3: Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093-0202, U.S.A.

Publication date: 2007-06-01

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