Abstract

Colonic probes usually show relatively uniform core temperatures in healthy terrestrial mammals. In contrast to this terrestrial homeothermic paradigm, some marine mammals display regional heterothermy in colonic temperatures. These marine mammals have stable, regionally specific temperatures at different positions along the colon -- typically a relatively cool region bordered by warmer temperatures. The observed differences are related to vascular adaptations that avoid elevated temperatures at their reproductive tissues.

We have shown that seals, dolphins, and manatees possess vascular structures that permit shunting of cooled superficial blood to positions deep within their bodies to avoid reproductive hypothermic insult. 26 These marine mammals divert cooled venous blood to reproductive organs before it is mixed with the core circulation co-opting extrinsic venous circulation that is separate from the intrinsic circulation of their reproductive organs. To measure the thermal effects of these vascular structures, we have used rectal probes housing linear arrays of five or more copper-constantan thermocouple^1,7 to measure temperatures simultaneously at several locations along the colon in the bottlenose dolphin (Tursiops truncatus) and the manatee (Trichechus manatus latirostris).

In the bottlenose dolphin, the distal colon follows the midline and passes between paired arteriovenous countercurrent heat exchangers that are found between the hypaxial muscles and the testes and uterus. Cooled superficial blood from the dorsal fin and flukes supplies the veins of these countercurrent heat exchangers, thus providing indirect cooling for these thermally sensitive tissues. The cooled venous plexuses also serve as direct heat exchangers between the hypaxial muscles and the testes and uterus. Temperatures within the region of the heat exchanger are lower than temperatures in front of and behind this region. Colonic temperatures adjacent to the heat exchanger were maximally 1.3°C cooler than temperature measured outside this region in the bottlenose dolphin. Temporary heating and cooling of the dorsal fin and flukes affected temperatures at the heat exchanger, but had little or no effect on temperatures outside this region.^1,7

In the Florida manatee, there are shallow hypogastric fossae in the abdominal wall that allow cooled venous blood from superficial thoracocaudal veins to enter venous plexuses in the dorsolateral abdominal cavity.³ These cooled venous plexuses function as direct heat exchangers between the dorsal aspect of the hypaxial muscles and the epididymides. The distal colon makes a bend towards the left side and follows the lateral margin of the abdominal cavity, coincidentally the colon passes over the region occupied by the left epididymis and its venous heat exchanger. Temperatures in male manatees adjacent to the heat exchanger were maximally 3.7°C cooler than temperatures measured in front of and behind this region. The temperature distribution changed as the colon shifted when the animal was rolled on its axis.⁸

The "U" shaped (warm-cool-warm) temperature profile we describe is an indicator of reproductive thermoregulation. An individual's profile may change with reproductive activity, season, physical activity, posture, and handling. Consideration of these normal healthy profiles should be given when measuring and interpreting body temperatures of diving mammals.

Acknowledgements

The authors wish to thank: G. Early, K. Matassa, and B. Wyman then at the New England Aquarium; T. Rowles at NMFS; W. Friedl and T. Williams then at NOSC, Hawaii; T. Grand, J. Mead, and C. Potter at the Smithsonian Institution; J. Reynolds at Eckerd College; D. Colbert, C. Manire, H. Rhinehart, and R. Wells at Mote Marine Lab; D. Murphy at Lowry Park Zoo; plus numerous support staff at these and other institutions.

References

1.  Pabst, D.A., S.A. Rommel, W.A. McLellan, T.M. Williams, and TIK. Rowles. 1995. Thermoregulation of the intra-abdominal testes of the bottlenose dolphin (Tursiops truncatus) during exercise Journal of Experimental Biology 198:221-226.

2.  Rommel, S.A., G.A. Early, K.A. Matassa, D.A. Pabst, and W.A. McLellan. 1995. Venous structures associated with thermoregulation of phocid seal reproductive organs. Anatomical Record 243"390-402.

3.  Rommel, S.A., D.A. Pabst, W.A. McLellan. (MS) Vascular Structures that Moderate Thermal Insult in the Male Florida Manatee (Trichechus manatus latirostris). Submitted to Anatomical Record.

4.  Rommel, S.A., D.A. Pabst, W.A. McLellan. 1998. Reproductive Thermoregulation in Marine mammals American Scientist 86:440-450.

5.  Rommel, S.A., D.A. Pabst, and W.A. McLellan. 1993. Functional Morphology of the Vascular Plexus Associated With the Cetacean Uterus. Anatomical Record 237:538-546.

6.  Rommel, S.A., D.A. Pabst, W.A. McLellan, J.G. Mead, and C.W. Potter. 1992. Anatomical Evidence for a Countercurrent Heat Exchanger Associated With Dolphin Testes. Anatomical Record. 232" 150-156.

7.  Rommel, S.A., D.A. Pabst, W.A. McLellan, T.M. Williams, and W.A. Friedel. 1994. Temperature regulation of the testes of the bottlenose dolphin (Tursiops truncatus); evidence from colonic temperatures. Journal of Comparative Physiology B 164:130-134.

8.  Rommel, S.A., D.A. Pabst, W.A. McLellan, C.A. Manire, D. Colbert, and D.D. Murphy (MS in prep.) Temperature Regulation of the Epididymides in the Florida Manatee (Trichechus manatus latirostris): Evidence from Colonic Temperatures.