Remora cranial vein morphology and its functional implications for attachment

Brooke E Flammang,Christopher P Kenaley

doi:10.1038/s41598-017-06429-z

Brooke E Flammang, Christopher P Kenaley

Open Access

https://doi.org/10.1038/s41598-017-06429-z

Copy DOI

Abstract

Remora fishes adhere to, and maintain long-term, reversible attachment with, surfaces of varying roughness and compliance under wetted high-shear conditions using an adhesive disc that evolved from the dorsal fin spines typical of other fishes. Evolution of this complex hierarchical structure required extensive reorganization of the skull and fin spines, but the functional role of the soft tissues of the disc are poorly understood. Here I show that remora cranial veins are highly-modified in comparison to those of other vertebrates; they are transposed anteriorly and enlarged, and lie directly ventral to the disc on the dorsum of the cranium. Ancestrally, these veins lie inside the neurocranium, in the dura ventral to the brain, and return blood from the eyes, nares, and brain to the heart. Repositioning of these vessels to lie in contact with the ventral surface of the disc lamellae implies functional importance associated with the adhesive mechanism. The position of the anterior cardinal sinus suggests that it may aid in pressurization equilibrium during attachment by acting as a hydraulic differential.

Highlights

Remoras (Echeneoidea) comprise a clade of fishes that have evolved an adhesive disc on the dorsal aspect of the head which permits them long-term reversible attachment to a variety of hosts of different roughness and body compliance[1,2,3,4,5,6]
Whereas previous research has investigated the development of the remora disc[7], adhesive force measurements[8,9], and the skeletal components contributing to the hierarchical mechanics of adhesion[8,10], little attention has been paid to the soft tissues that contribute to remora adhesion mechanics[12]
Dissection of a euthanized, fresh remora revealed large diameter blood vessels lying dorsal to the skull and in contact with the ventral side of the lamellae and associated musculature of the adhesive disc. This vasculature was better visualized through reconstruction of computed microtomography scans of remora specimens perfused with iodixanol, which revealed that these exceptionally large cranial veins are located within a space situated between the pectinated lamellae of the disc and the dorsal aspect of the cranium (Fig. 1), indicating that when the lamellae are erected, the cranial veins and their overlying epithelium constitute the roof of each lamellar compartment when attached to a host organism

Summary

Results and Discussion

Dissection of a euthanized, fresh remora revealed large diameter blood vessels lying dorsal to the skull and in contact with the ventral side of the lamellae and associated musculature of the adhesive disc. I hypothesize that the antero-dorsally transposed position of the ACS allows it to function as a hydraulic differential[20], promoting equalization of pressure among lamellar compartments at the time of attachment, thereby eliminating localized relative pressure gradients that would increase fluid seep and cause suction failure. The hierarchical adhesive mechanism of some geckos relies upon a fluid pressure differential; the reticular network of enlarged blood vessels in the lamellar plates allows deformation of scansors along multiple axes at a single time, thereby promoting adhesive contact on irregular surfaces[20,24,25] It is worth noting, that the ACS only lies deep to the anterior 70% of the disc; the more caudal 30% of the disc lies dorsal to the body. The evolution of this unique morphology, that would otherwise seem constrained given the nature of its physiology, and which places a large, thin-walled vein in a very superficial position anatomically, underlies the functional importance of the ACS in the remora adhesive mechanism

Experimental Procedures

Author Contributions

Additional Information