Vascular adaptations for heat conservation in the tail of Florida manatees (Trichechus manatus latirostris)

Abstract

Although Florida manatees (Trichechus manatus latirostris) have relatively low basal metabolic rates for aquatic mammals of their size, they maintain normal mammalian core temperatures. We describe vascular structures in the manatee tail that permit countercurrent heat exchange (CCHE) to conserve thermal energy. Approximately 1000 arteries juxtaposed to 2000 veins are found at the cranial end of the caudal vascular bundle (CVB); these numbers decrease caudally, but the 1:2 ratio of arteries to veins persists. Arterial walls are relatively thin when compared to those previously described in vascular countercurrent heat exchangers in cetaceans. It is assumed that CCHE in the CVB helps manatees to maintain core temperatures. Activity in warm water, however, mandates a mechanism that prevents elevated core temperatures. The tail could transfer heat to the environment if arterial blood delivered to the skin were warmer than the surrounding water; unfortunately, CCHE prevents this heat transfer. We describe deep caudal veins that provide a collateral venous return from the tail. This return, which is physically outside the CVB, reduces the venous volume within the bundle and allows arterial expansion and increased arterial supply to the skin, and thus helps prevent elevated core temperatures.

Fig. 1

Ventral photograph of the branching pattern of a right intercostal artery proximal to the vertebral column in the dorsal aspect of the manatee pleural cavity (LPZ100942). The parietal pleura and some fat have been removed; the manatee's head is to the left. The division of vessels in the manatee does not produce a tree-like pattern but resembles the arrangement of a brush or broom, called a vascular bundle. Each of the small arteries is approximately 0.5 mm in diameter and number between 30 and 40 at the proximal end of each intercostal space.

Fig. 2

Ventral and cross-sectional schematics of the arteries and veins in the caudal region of the manatee. (A) There is a relatively simple arterial pattern in the thoracic region, in contrast to the arterial patterns in the region of and caudal to the last two ribs. Arteries branch from the aorta to form a thin, fan-shaped array of arteries (the iliac arterial plexus), each of which is about 0.75 cm in diameter. Caudal to the relatively two-dimensional iliac arterial plexus there is a three-dimensional array that extends into the space between the chevron bones (chevron canal) along the ventral aspects of the caudal vertebrae. (B) The veins also have a relatively simple pattern in the thorax, which develops into a more complex pattern in the region of the last two ribs. The caudal venae cavae are paired about mid thorax caudad; they may completely cover the ventral aspect of the aorta in some specimens. The two-dimensional iliac venous plexus extends laterally from the venae cavae over the ventral aspect of the caudal abdomen. Caudal to the iliac venous plexus is a roughly triangular array that extends within the chevron canal. (C) Juxtaposition of numerous small-diameter arteries and veins produces an iliac vascular bundle in the caudal abdomen and an arteriovenous caudal vascular bundle within the chevron canal.

Fig. 3

(A) Ventral photograph of an acrylic cast of the arteries in the cranial portion of the caudal vascular bundle (MSE9833). (B) Ventral photograph of latex-injected, paired venae cavae, iliac venous plexus, and caudal vascular bundle (MNW9718). (C) Photograph of a cross-section of the central portion of the CVB cranial to the region where it entered the chevron canal (MNW9802). The arteries were injected with red latex and the veins with blue latex; the injections were less complete in the lower portion of the cross-section. Over 875 arteries are visible in this image. The large, thick-walled artery in the lower half of the image is the vestige of the caudal aorta.

Fig. 4

Photomicrograph (H&E stain) of a transverse section of the caudal vascular bundle (CVB) in a Florida manatee. Some of the vessels, particularly the arteries, have blood in them. Each artery (A) is surrounded by a rosette of shared veins (V); this arrangement produces an optimal pattern for countercurrent exchange. Within the CVB, frequent anastomoses (An) between veins, occasional anastomoses between arteries, and no anastomoses between arteries and veins were observed.

Fig. 5

Ventral schematic view of the deep caudal veins in the tail of the manatee. These veins lie on the ventral aspects of the transverse processes of the caudal vertebrae and are surrounded by the hypaxial muscles. These veins are collateral to the warmed venous return of the caudal vascular bundle and thus bypass this countercurrent heat exchanger.