The Spleen as an Unlikely Source of red blood cells during activity in fishes

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Journal of Experimental Biology

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We read with interest the paper by Brijs et al. (2020) regarding the ‘blood-boosting’ properties apparently exhibited by the Antarctic notothenioid fish (Pagothenia borchgrevinki). Although the data provide additional insights into the physiology of an extreme cold-adapted fish, we believe the authors have drawn erroneous conclusions about the mechanisms involved with this ‘blood-boosting’ phenomenon. The authors conclude that the spleen sequesters enough red blood cells (RBCs) to increase the haematocrit (Hct) and, therefore, blood oxygen carrying capacity in fed and exercise states. Further, the authors posit the spleen holds these RBCs in reserve to reduce blood viscosity until additional oxygen is needed to support increases in metabolic rate. In our view, the increases in Hct in P. borchgrevinki can be primarily explained by an alternative mechanism that the authors did not consider in their analysis: elevated blood pressure increases plasma efflux from the vascular to the interstitial space, thus increasing the fraction of RBCs in the vascular space (i.e. Hct).

We present two arguments against a role for the spleen in providing a significant contribution to increased Hct in P. borchgrevinki. Our first argument is based on the principle of conservation of mass. Brijs et al. (2020) used uninstrumented fish to examine changes in spleen volume at rest, after feeding and following enforced exercise. The comparisons are partly confounded by significant differences in body mass between groups. We have plotted the authors' data for unfed and fed animals in resting and exercised states to show the significant relationships between spleen mass and body mass. If we compare a 74 g fish for both groups, spleen mass for resting fish is 0.365 g and is 0.213 g after exercise (Δ spleen mass=0.152 g). Can this change in spleen mass account for the changes in Hct observed by the authors? If we assume a blood volume of 5% of body mass, for a 74 g fish blood volume is 3.7 g (=3.7 ml, assuming blood has a density of 1 g ml−1). The average Hct was 15.8% and 27.1% for resting and exercised fish, respectively. The mass of RBCs for this blood volume is therefore 0.585 g (rest) and 1.003 g (exercise) with a difference of 0.418 g (ml). It is clear that changes in spleen volume cannot account for the mass of RBCs added to the vascular space during exercise. The changes in spleen mass account for approximately 36% of the change in RBC mass with the remaining 64% of RBC unaccounted for; with unfed fish, Hct changes from 8.6% to 25.1% and the non-splenic contribution is larger (76%). We also note that for resting fish (unfed vs fed), Hct increased from ∼9% to ∼21%, but absolute spleen mass increased, rather than decreased, a further indication that non-splenic mechanisms account for the increased Hct.


© 2020. Published by The Company of Biologists Ltd

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