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Thermoregulation in Feeding Baleen Whales: Morphological and Physiological Evidence

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Thermoregulation in Feeding Baleen Whales: Morphological and Physiological Evidence Aquatic Mammals 2001, 27.3, 284–288 Thermoregulation in feeding baleen whales: Morphological and physiological evidence John E. Heyning Natural History Museum of Los Angeles County, 900 Exposition Blvd., Los Angeles, CA. 90007, USA Abstract The insulating blubber often is considered an inert insulative covering. In reality, by varying Gray whales (Eschrichtius robutus) expose their blood flow, the insulative property of blubber can immense oral cavities repeatedly to frigid waters be bypassed and hence thermoregulation is quite when feeding. Morphological structures for heat dynamic. Many of the larger cetaceans have no conservation in the tongues of gray whales are trouble staying warm even in polar waters described here in detail. Numerous individual coun- (Hokkanen, 1990); in fact, dumping heat could be tercurrent heat exchangers converge at the base more challenging under some conditions. Even for of the tongue to form a bilateral pair of vascu- smaller species, there are times when certain organs lar bundles called the lingual rete. Temperature must be actively cooled to prevent tissue damage. measurements taken from a live captive gray whale Because with any endotherm, a cetacean needs to calf indicated that more heat could be lost through avert excess heat loss and also regulate its core body the blubber layer over the body than through the temperature in relation to its metabolic rate and the tongue, despite the fact that the tongue is far more ambient temperature (Parry, 1949). vascularized and has much less insulation. Hence, The blubber effectively insulates the majority these heat exchangers substantially reduce heat of the body surface and the countercurrent heat loss when these whales feed in cold waters. The exchangers in the vascular system of the fins and evolution of these structures was a physiological flukes of whales and dolphins serve to conserve core prerequisite for baleen whale breeding. body temperature. However, a critical anatomical region relating to thermoregulation was overlooked Key words: mysticete, thermoregulation, counter- for decades. Baleen whales (suborder Mysticeti) current mechanism, rete, gray whale, tongue. have cavernous mouths to accommodate the large filtering surface comprised of baleen. Whereas, the Introduction blubber enshrouding the head provides suitable insulation when the mouth is closed, the inner The oceans and seas are energetically challenging surface of the mouth is highly vascualarized and environments for endotherms because water con- relatively uninsulated. Furthermore, most species of ducts heat away at approximately 25 times the rate baleen whales feed in the cold waters of high of air. There are three primary mechanisms by latitudes. Therefore, feeding exposes the large which cetaceans regulate their body temperature. surface area of the tongue to the cold polar and The first is through insulation, for which cetaceans subpolar waters these whales inhabit. rely on the subdermal layer of adipose tissue coined Ryg and colleagues (1993) first noted that the ‘blubber’ by early whalers. Second, is to regulate oral cavity of feeding baleen whales represents a blood flow to the surface of the skin, especially major surface for heat loss; however, they lamented through the extremities. All cetaceans have an that there were no measurements to quantify this extremely complex vascular system to achieve loss. Small countercurrent heat exchangers have such regulation. Thirdly, the metabolic rate can be been described for the gums and palate of fin increased to generate more heat for the system. whales, Balaenoptera physalus (Utrecht, 1958). The Whether or not any cetaceans have an elevated narrow palate of the right whale has also been basal metabolic rate is controversial (e.g. Lavigne suggested as a site for heat dumping (Ford & et al., 1986; Kastings et al., 1989; Kastings, 1991; Kraus, 1992) although Heyning, et al. (1993) Innes & Lavigne, 1991). noted that the palates of right whales lacked the 2001 EAAM Thermoregulation in feeding baleen whales 285 specializations necessary to serve as an important of countercurrent heat exchangers, yet were per- site of heat loss. plexed as to the function of these vascular bundles. The purpose of this report is to provide: 1) more The first author to ascribe a function to countercur- details of the previous study by Heyning & Mead rent heat exchangers in marine mammals was Parry (1997) on countercurrent heat exchangers in the (1949) who noted that by shunting arterial heat into oral cavity; 2) an overview of thermoregulation; 3) a the ‘accompanying venules’ that heat would be context for the oral cavity of baleen whales, and short-circuited back to the body core. Parry’s(op 4) a comparative context among baleen whales to cit.) observations were of the superficial vascular understand the distribution and evolution of these system along the entire body. Far more impressive important structures. countercurrent heat exchangers subsequently have been found associated with various extremities and organ systems. Materials and Methods Countercurrent heat exchangers function by con- ducting heat from warm arterial blood coming from Heyning & Mead (1997) dissected two freshly dead the body core to cool venous blood typically drain- gray whale calves. The tongue of the smaller calf ing the body surface (Scholander, 1958). This is (LACM 88981; 3.98 m) was transversely sectioned accomplished by situating an artery traveling to the at about 2 cm intervals and probes were inserted body surface adjacent to the veins returning from into the blood vessels to trace their course. The in that cool extremity. The warm arterial blood trans- situ architecture of the lingual rete of the larger calf fers its heat by simple conduction to the adjacent (LACM 92044; 5.25 m) was revealed by superficial cool venous blood. In this way, body warmth is to deep dissections to observe the connection of this re-circulated back to the body core vis a vis the plexus to the cranial-cervico vascular system. venous blood prior to losing heat to the environ- I measured the surface temperature of the ment. The classic countercurrent heat exchangers tongue and the skin of the head and neck of a live consist of a central arteriole surrounded by a plexus gray whale calf (JJ) during a series of feedings. of small venules. This architecture was coined the Temperature measurements were obtained using a peri-arterial venous retia by Elsner et al. (1974), a Raynger PM model PM313tru remote thermal sen- term which best describes the complex architecture sor held within 1 m of the target. Measurements of this network of interwoven blood vessels. were made when the calf briefly lifted its head out of The fins and flukes of whales and dolphins, the water at the beginning and the end of a feeding essential for locomotion and manoeuvering, are session. Each recording was based on several indi- potentially significant sites of heat loss in cold vidual measurements made over a period of several waters because they lack insulative blubber and seconds. Measurements were taken after most of have relatively large surface areas. Conversely, it the water dripped-off, but a thin sheen of water has been observed that when a cetacean is held-out remaining upon the body surface. The temperature of water, these extremities overheat relative to the measurements from the neck region did not change torso skin temperature because the animal attempts from its initial reading until the animal re- dump excess heat through its appendages (Elsner submerged after at least 1 min of exposure to air. et al., 1974). This suggested that any biases in measures from the Recent studies (see Pabst et al., 1998 for a wet surface area should be minor and apply equally review) have demonstrated that countercurrent heat to all measurements. exchangers are responsible for cooling the testes to The first measurements were taken when the calf promote spermatogenesis or the ovaries to prevent was about four months old. At this time the am- hyperthermia in the fetus. Cool blood from the bient water temperature was 19.5)C. A second series flukes via the lateral caudal arteries and blood from of measurements were taken when the calf was the lateral abdominal subcutaneous veins, which about eight months old in ambient water tempera- drain the dorsal fin, conjoin and then divide into a ture of 12.5)C. In both temperature regimes, the series of small veins forming a venous plexus in the relative temperature relationship between the region of the gonads. ambient water, body surface, and tongue surface Like most baleen whales, gray whales have rela- did not change further suggesting that measurement tively large mouths and migrate to cold waters for biases were minor. feeding during the summer. Heyning and Mead (1997) calculated that the surface area of tongue of Results and Discussion a gray whale represents approximately 5% of the surface area of the body, excluding the extremities. Anatomical evidence Thus, the oral cavity should be an important region Walmsley (1938) and other early workers identified for thermoregulation. Notwithstanding feeding, and clearly described the anatomical configuration theoretical calculations predict that the blubber 286 J. E. Heyning layer of gray whales should effectively insulate tissue about 2 cm thick in the calves we dissected. A these whales even in cold polar waters (Hokkanen, similar, but even more distinct, enveloping fatty 1990). layer of the tongue is clearly visible in a transverse Scattered throughout the tongue Heyning and section of the tongue of the obligatory Arctic Mead (op cit.) observed numerous individual coun- species, the bowhead whale (Balaena mysticetus) tercurrent heat exchangers consisting of a single (see Haldiman & Tarpley, 1993; Fig.4.17B). This peri-arterial venous retia. These individual counter- outer layer of adipose tissue could be function- current heat exchangers are about 0.7 cm in diam- ally analogous to the blubber layer of the body, eter. These blood vessels are oriented in planes so providing at least some insulation for the tongue.
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