Role of the left aortic arch and blood flows in embryonic American alligator (Alligator mississippiensis)

Abstract

All embryonic and fetal amniotes possess a ductus(i) arteriosus(i) that allows blood to bypass the pulmonary circulation and the non-functional lungs. The central hemodynamic of embryonic reptiles are unique, given the additional systemic aorta that allows pulmonary circulatory bypass, the left aorta (LAo). The LAo exits in the right ventricle or ‘pulmonary side’ of reptilian hearts in both embryos and adults, but its functional significance in ovo is unknown. This study investigated the role of the LAo in embryonic American alligators by surgically occluding the LAo and measuring oxygen consumption and, in addition, measured hemodynamic responses to hypoxia in embryonic alligators. We measured systemic cardiac output and primary chorioallantoic membrane (CAM) artery blood flow for normoxic and hypoxic-incubated (10% O2) American alligator embryos (Alligator mississippiensis). Chronic blood flow (1–124 h) in the primary CAM artery for hypoxic-incubated embryos (92 ± 26 ml min−1 kg−1) was elevated when compared with normoxic-incubated embryos (29 ± 14 ml min−1 kg−1, N = 6; P = 0.039). For hypoxic-incubated embryos, acute LAo blood flow (49.6 ± 24.4 ml min−1 kg−1) was equivalent to the combined flow of the three systemic great vessels that arise from the left ventricle, the right aorta, common carotid and subclavian arteries (43.6 ± 21.5 ml min−1 kg−1, N = 5). Similarly, for normoxic-incubated embryos, LAo blood flow (27.3 ± 6.6 ml min−1 kg−1) did not statistically differ from the other three vessels (18.4 ± 4.9 ml min−1 kg−1, N = 5). This study contains the first direct test of LAo function and the first measurements of blood flow in an embryonic reptile. These data support the hypotheses that embryonic alligators utilize the LAo to divert a significant amount of right ventricular blood into the systemic circulation, and that CAM blood flow increases following chronic hypoxic conditions. However, surgical occlusion of the LAo did not affect egg supporting the hypothesis that the LAo of reptiles is not critical to maintain in ovo oxygen consumption.Electronic supplementary materialThe online version of this article (doi:10.1007/s00360-010-0494-6) contains supplementary material, which is available to authorized users.

Hypoxic alligator embryos: Chronic hypoxia, catecholamine levels and autonomic responses of in ovo alligators

“…Given this physical alteration, chronic overstimulation of β-adrenoreceptors may be necessary to maintain adequate cardiac output and perfusion, while balancing the need to maintain adequate peripheral resistance. Stimulation of β-adrenoreceptors on the heart is responsible for maintaining embryonic cardiac output, and H10 embryos have previously shown increased blood flow to the CAM (Eme et al, 2011a), suggesting that overstimulation of β-adrenoreceptors may be partially responsible for increased CAM blood flow. In addition, chronic hypoxic incubation of chickens results in increased cardiac and vascular sensitivity to -stimulation (Lindgren and Altimiras, 2009;Lindgren et al, 2011), as well as increased plasma noradrenaline (Lindgren et al, 2011).…”

“…Unlike birds and mammals, the low metabolic rate and lower incubation temperature for crocodilian embryos may preclude any functional need to accelerate development of such variables. To date, only the likely interconnected increased vascularization of the CAM and increased blood flow to the CAM in hypoxic alligator embryos seem likely to aid in increased embryo oxygenation (Corona and Warburton, 2000;Eme et al, 2011a).…”

“…Chronic regional hypoxia increases vascularization of the CAM in alligators (Corona and Warburton, 2000), and this accompanied addition of parallel vascular beds could be a mechanism leading to an observed decrease in chorioallantoic resistance and pressure (Crossley and Altimiras, 2005). This decreased pressure could account for increased blood flow to the CAM in chronic hypoxic alligator embryos, compared to normoxic embryos (Eme et al, 2011a). Therefore, the cardiovascular system of the developing reptilian embryo is susceptible and responsive (plastic) to changes in nest atmospheric gas composition.…”

“…In chronically hypoxic-incubated alligator embryos, putative mechanisms exist for the observed reduction in arterial pressure -increased CAM vascularization (Corona and Warburton, 2000), as well as the observed increased blood flow to the CAM -ventricular hypertrophy and decreased CAM pressure (Crossley and Altimiras, 2005;Eme et al, 2011a). However, the mechanism(s) that underlie alligator embryo's documented bradycardia in response to acute hypoxia (10% O 2 ), as well as the bradycardia measured in normoxia (21% O 2 ) for embryos incubated in chronic hypoxia (10% O 2 ) remain in question (Crossley and Altimiras, 2005) and could be caused by altered nervous control and/or humoral control.…”

The phylogeny and ontogeny of autonomic control of the heart and cardiorespiratory interactions in vertebrates

“…Changes in f H during development have been described in representative species from each of the major reptilian clades, excluding Sphenodontia (Fig. 4), but measurements of blood flow have only been conducted in embryonic alligators (Eme et al, 2011a). Embryonic heart mass has been suggested to be an index of stroke volume during reptilian development (Birchard and Reiber, 1996;Crossley and Altimiras, 2000) so that changes in heart mass, in combination with measurement of f H , may provide an index of the changes in cardiac output accompanying development, enabling study of its control.…”