Right-to-left shunt has modest effects on CO2 delivery to the gut during digestion, but compromises oxygen delivery

Abstract

By virtue of their cardiovascular anatomy, reptiles and amphibians can shunt blood away from the pulmonary or systemic circuits, but the functional role of this characteristic trait remains unclear. It has been suggested that right-to-left (R-L) shunt (recirculation of systemic blood within the body) fuels the gastric mucosa with acidified and CO 2 -rich blood to facilitate gastric acid secretion during digestion. However, in addition to elevating P CO2 , R-L shunt also reduces arterial O 2 levels and would compromise O 2 delivery during the increased metabolic state of digestion. Conversely, arterial P CO2 can also be elevated by lowering ventilation relative to metabolism (i.e. reducing the air convection requirement, ACR). Based on a mathematical analysis of the relative roles of ACR and R-L shunt on O 2 and CO 2 levels, we predict that ventilatory modifications are much more effective for gastric CO 2 supply with only modest effects on O 2 delivery. Conversely, elevating CO 2 levels by means of R-L shunt would come at a cost of significant reductions in O 2 levels. The different effects of altering ACR and R-L shunt on O 2 and CO 2 levels are explained by the differences in the effective blood capacitance coefficients.

Cardiovascular shunting in vertebrates: a practical integration of competing hypotheses

“…However, the proposal that the R–L shunt facilitates digestion is problematic because the shunted blood is low in oxygen and thus lower oxygen delivery would coincide with an elevated oxygen consumption due to the specific dynamic action (SDA) response (Busk et al ., ). Modelling of gas exchange shows that R–L shunts exert rather small effects on P CO 2 because CO 2 has such high solubility in blood (Malte et al ., ), and these predictions were verified by experimental data (Conner et al ., ). Consequently, it seems very doubtful that a R–L shunt could serve a role in stimulating gastric acid secretion.…”

“…These attributes led to the conclusion that cardiovascular shunts evolved through natural selection, rather than representing evolutionary relics or failed evolutionary experiments. Yet, the answer to the question ‘What is the purpose of cardiovascular shunts?’ has remained elusive, fueling a key debate in contemporary comparative physiology (Burggren, ; Hicks & Wang, , ; Farmer & Carrier, ; Wang et al ., ; Farmer & Hicks, ; Hicks, ; Wang & Hicks, , ; Wang, Altimiras, & Axelsson, ; Krosniunas & Hicks, ; Farmer et al ., ; Eme et al ., , ; Joyce et al ., ; Malte et al ., ). Researchers have used ever more sophisticated experimental approaches, with the goal of identifying ‘the reason’ underpinning cardiovascular shunting as an adaptation.…”

“…The recognition of multiple shunt functions evoked under multiple environmental conditions also means that experiments must be designed specifically to explore potential synergies and conflicts. One example of such an approach calculated shunting effects mathematically while simultaneously considering two major proposed functions of intracardiac shunting in reptiles – digestion and oxygen transport (Malte et al ., ). A prediction of this study (that elevating CO 2 delivery to the gut would come at a cost of significant reductions in O 2 transport) is less important than the fact that the authors actually simultaneously considered multiple, conflicting shunt functions.…”

“…Yet, the answer to the question 'What is the purpose of cardiovascular shunts?' has remained elusive, fueling a key debate in contemporary comparative physiology (Burggren, 1987;, 2012Farmer & Carrier, 2000;Wang et al, 2001;Farmer & Hicks, 2002;Hicks, 2002;Wang & Hicks, 2002Wang, Altimiras, & Axelsson, 2002;Krosniunas & Hicks, 2003;Farmer et al, 2008;Eme et al, 2009Eme et al, , 2010Joyce et al, 2016;Malte et al, 2017). Researchers have used ever more sophisticated experimental approaches, with the goal of identifying 'the reason' underpinning cardiovascular shunting as an adaptation.…”

Does the left aorta provide proton-rich blood to the gut when crocodilians digest a meal?

“…The fundamental hypothesis of the R-L shunt serving to deliver CO 2 -rich blood to digestive organs was recently questioned on theoretical grounds. Based on mathematical modeling, Malte et al (2017) argued that the R-L shunt would be rather ineffective at elevating arterial partial pressure of CO 2 (P CO2 ), and that an increased R-L shunt would compromise oxygen delivery during digestion. Instead, it was reasoned that the hypoventilation, which characterizes the postprandial state (Wang et al, 2001), would be a much more effective mechanism to elevate arterial P CO2 with minimal effect on arterial oxygen levels (Malte et al, 2017).…”