Effects of forced diving on the spleen and hepatic sinus in northern elephant seal pups

Abstract

In phocid seals, an increase in hematocrit (Hct) accompanies diving and periods of apnea. The variability of phocid Hct suggests that the total red cell mass is not always in circulation, leading researchers to speculate on the means of blood volume partitioning. The histology and disproportionate size of the phocid spleen implicates it as the likely site for RBC storage. We used magnetic resonance imaging on Northern elephant seals to demonstrate a rapid contraction of the spleen and a simultaneous filling of the hepatic sinus during forced dives (P < 0.0001, R 2 ‫؍‬ 0.97). The resulting images are clear evidence demonstrating a functional relationship between the spleen and hepatic sinus. The transfer of blood from the spleen to the sinus provides an explanation for the disparity between the timing of diving-induced splenic contraction (Ϸ1-3 min) and the occurrence of peak Hct (15-25 min). Facial immersion was accompanied by an immediate and profound splenic contraction, with no further significant decrease in splenic volume after min 2 (Tukey-Kramer HSD, P ‫؍‬ 0.05). At the conclusion of the dive, the spleen had contracted to 16% of its predive volume (mean resting splenic volume ‫؍‬ 3,141 ml ؎ 68.01 ml; 3.54% of body mass). In the postdive period, the spleen required 18 -22 min to achieve resting volume, indicating that this species may not have sufficient time to refill the spleen when routinely diving at sea, which is virtually continuous with interdive surface intervals between 1 and 3 min. P hocid seals exhibit a higher hematocrit (Hct) during apnea and diving than during periods of eupneic respiration (1-4). This variation in red cell mass indicates that seals have some method of sequestering red cells during nonapneic events. Bryden and Lim (5) found the Hct values of elephant seal pups to be highly variable and suggested that the spleen acts as a dynamic reservoir for erythrocytes, releasing RBCs into general circulation when required. Qvist et al. (2) recorded a distinct rise in Weddell seal Hct during diving and suggested that the total red cell mass is partitioned between general circulation and the splenic reservoir. The concept of splenic red cell storage is well accepted by many researchers, and a diving-induced sympathetic vasoconstriction is thought to be the stimulus for splenic contraction and subsequent injection of oxygenated RBCs into circulation (2, 4, 6, 7). Strong evidence supports this line of reasoning. Histological and physiological data collected on seal spleens indicate that the organ is capable of considerable RBC storage and that it reacts to catecholamine stimulation (6-9). The ability of the phocid spleen to concentrate RBCs is supported by high Hct values obtained from splenic venous blood during catecholamine-induced contraction (88-93% in hooded seals; 82-88% in harp seals; ref. 7). Ultrasound imaging in Weddell seals demonstrates a correlation of the diving-induced rise in Hct with a postdive reduction in spleen size (6).Dive and postdive catecholamine levels collected fro...

Blood oxygen depletion during rest-associated apneas of northern elephant seals (Mirounga angustirostris)

“…Castellini (Castellini, 1994) noted that Hct remained elevated during sequential apnea-eupnea cycles (as were characteristic of the seals in our study), and that it was necessary for the seal to be awake and breathing for several minutes after these cycles before Hct would decrease significantly. Two other studies have documented that splenic re-expansion times observed after dives (6-9·min half-times) (Hurford et al, 1996) and forced submersions (18-22·min for complete re-expansion) (Thornton et al, 2001) are long in comparison with eupneic intervals. The eupneic phases in our study generally lasted only a few minutes, with much of that time characterized by intermittent, slow breaths and usually with the seal still apparently asleep.…”

Erythropoietin elevates but not voluntary wheel running in mice

“…One longer-term effect of exercise is an increased [Hb] (triggered via tissue hypoxia). However, in some diving mammals, such as the Weddell seal (Hurford et al, 1996) and northern elephant seal (Thornton et al, 2001), and in some terrestrial mammals, including the horse (Persson et al, 1973;Thomas et al, 1981), dog (Vatner et al, 1974) and human being (Laub et al, 1993;Stewart et al, 2003), [Hb] can be increased acutely by contraction of the spleen ('autotransfusion').…”

“…One longer-term effect of exercise is an increased [Hb] (triggered via tissue hypoxia). However, in some diving mammals, such as the Weddell seal (Hurford et al, 1996) and northern elephant seal (Thornton et al, 2001), and in some terrestrial mammals, including the horse (Persson et al, 1973;Thomas et al, 1981), dog (Vatner et al, 1974) and human being (Laub et al, 1993;Stewart et al, 2003), [Hb] can be increased acutely by contraction of the spleen ('autotransfusion').In human beings, as in the HR lines of mice (see above) and in a rat line bred for high treadmill endurance (Gonzalez et al, 2006) for non-athletes (Lucia et al, 2001). However, recent studies of variation in maximal aerobic performance suggest that neurobiological attributes (Kayser, 2003;Noakes, 2007;Noakes, 2009), including focus of concentration (Rose and Parfitt, 2007) and altered perception of exertion (Baden et al, 2005), also play a role in performance ability.…”

Apnea stimulates the adaptive response to oxidative stress in elephant seal pups

“…It has been consistently found that breath-holding with face immersion produces a more profound response (greater bradycardia and hypometabolism) than breathholding alone [for a complete review see Elsner (Elsner, 1999)]. Also, the decrease in circulating xanthine, HX and XO activity during the first minute of the voluntary submersions can be explained by the fact that submersion produces an immediate and profound splenic contraction without any further significant decrease in splenic volume after the second minute, resulting in higher hematocrit in venous ciruclation at the beginning of a submersion than during eupnea (Thornton et al, 2001).…”