Embryonic hypoxia programmes postprandial cardiovascular function in adult common snapping turtles (Chelydra serpentina)

Abstract

Reduced oxygen availability (hypoxia) is a potent stressor during embryonic development, altering the trajectory of trait maturation and organismal phenotype. We previously documented that chronic embryonic hypoxia has a lasting impact on the metabolic response to feeding in juvenile snapping turtles (Chelydra serpentina). Turtles exposed to hypoxia as embryos [10% O 2 (H10)] exhibited an earlier and increased peak postprandial oxygen consumption rate, compared with control turtles [21% O 2 (N21)]. In the current study, we measured central blood flow patterns to determine whether the elevated postprandial metabolic response in H10 turtles is linked to lasting impacts on convective transport. Five years after hatching, turtles were instrumented to quantify systemic ( _ Q sys ) and pulmonary ( _ Q pul ) blood flows and heart rate ( f H ) before and after a ∼5% body mass meal. In adult N21 and H10 turtles, f H was increased significantly by feeding. Although total stroke volume (V S,tot ) remained at fasted values, this tachycardia contributed to an elevation in total cardiac output ( _ Q tot ). However, there was a postprandial reduction in a net left-right (L-R) shunt in N21 snapping turtles only. Relative to N21 turtles, H10 animals exhibited higher _ Q sys due to increased blood flow through the right systemic outflow vessels of the heart. This effect of hypoxic embryonic development, reducing a net L-R cardiac shunt, may support the increased postprandial metabolic rate we previously reported in H10 turtles, and is further demonstration of adult reptile cardiovascular physiology being programmed by embryonic hypoxia.

Analysis of vascular mechanical properties from the yellow anaconda indicates increased elasticity and distensibility of the pulmonary artery during digestion

“…The only study that measured chronic changes of pulmonary blood flow in a conscious reptile after feeding showed that the common snapping turtle, Chelydra serpentina, reduces the left to right cardiac shunt (i.e. systemic bypass of the blood flow), indicating that systemic resistance decreases more than pulmonary resistance (Wearing et al, 2017). This hints at the possibility that smooth muscle regulation during the postprandial period plays a more important role in regulating the systemic vasculature, where we observed no changes in mechanical properties of the dorsal aorta, than in the pulmonary arteries.…”

Physiological plasticity in lizard embryos exposed to high‐altitude hypoxia

“…Whether physiological adjustments that promote successful development in hypoxia‐incubated embryos affect post‐hatching performance and survival is as of yet unclear (but see Wearing, Conner, Nelson, Crossley, and Crossley ()). However, constraints on yolk utilization, and hence hatchling size, may have important fitness consequences (Sinervo, ; Warner, ).…”

Transplanting gravid lizards to high elevation alters maternal and embryonic oxygen physiology, but not reproductive success or hatchling phenotype

“…The long-term effects of hypoxia exposure during development on phenotype and fitness at later life-history stages remain important research questions. For example, development in hypoxia has long-term effects on post-hatching cardiovascular phenotypes in snapping turtles (Chelydra serpentina; Wearing et al, 2016Wearing et al, , 2017, decreases swimming performance in snakes (Natrix maura; F.A. and J.S., unpublished results), and impacts cognitive ability in lizards (Eremias argus; Sun et al, 2014).…”

“…Under certain conditions, oxygen restrictions can also result in depressed metabolism, decreased growth and reduced survivorship to hatching (Iungman and Piña, 2013;Warburton et al, 1995). These early developmental effects can persist into later life phenotypes (Sun et al, 2014;Wearing et al, 2017).…”