Rates of oxygen uptake increase independently of changes in heart rate in late stages of development and at hatching in the green iguana, Iguana iguana

Abstract

Oxygen consumption (VO), heart rate (f), heart mass (M) and body mass (M) were measured during embryonic incubation and in hatchlings of green iguana (Iguana iguana). Mean f and VO were unvarying in early stage embryos. VO increased exponentially during the later stages of embryonic development, doubling by the end of incubation, while f was constant, resulting in a 2.7-fold increase in oxygen pulse. Compared to late stage embryos, the mean inactive level of VO in hatchlings was 1.7 fold higher, while f was reduced by half resulting in a further 3.6 fold increase in oxygen pulse. There was an overall negative correlation between mean f and VO when data from hatchlings was included. Thus, predicting metabolic rate as VO from measurements of f is not possible in embryonic reptiles. Convective transport of oxygen to supply metabolism during embryonic incubation was more reliably indicated as an index of cardiac output (CO) derived from the product of f and M. However, a thorough analysis of factors determining rates of oxygen supply during development and eclosion in reptiles will require cannulation of blood vessels that proved impossible in the present study, to determine oxygen carrying capacity by the blood and arteriovenous oxygen content difference (A-V diff), plus patterns of blood flow.

Developmental staging table of the green iguana

“…Popularly known as green iguana, Iguana iguana iguana, is widely distributed in Central and South America, occurring from northern Mexico to south‐eastern Paraguay and Brazil (Barten, ; Blair, ; Campos & Desbiez, ; Swanson, ). Green iguana was established as an experimental species by several biological studies (Butler & Northcutt, ; Foster & Hall, ; Janke, Erpenbeck, Nilson, & Arnason, ; Sartori, Abe, Crossley, & Taylor, ; Sartori, Taylor, Abe, & Crossley, ), although details of its embryonic development had not been widely explored.…”

Convective oxygen transport during development in embryos of the snapping turtle Chelydra serpentina

“…However, the size of the heart relative to the size of the embryo decreased from 0.46% at 50% incubation to 0.31% at 90% incubation (Table 1). This is also the case for the turtles Emys orbicularis (from approximately 0.56% at 50% incubation to 0.31% when close to hatching; Nechaeva et al, 2007) and Lepidochelys olivacea (from 0.46% at 70% incubation to 0.39% at 90%; Crossley et al, 2017a), and for the lizard Iguana iguana (from 0.35% at 30% incubation to 0.26% at 90% incubation; Sartori et al, 2017). This difference in heart growth, when compared with the body mass increase, could be offset to some extent by the reduction in tissue oxygen requirement of the embryo, reflected by the decrease in mass-specific VȮ 2 (Sartori et al, 2017) and a consequent decrease in massspecific O 2 pulse, as described for the marine iguana by Butler and colleagues (2002).…”

“…f H of snapping turtle embryos decreased significantly at the end of incubation, a common pattern of members of the order Testudines (Alvine et al, 2013;Birchard and Reiber, 1996;Crossley, 1999;Birchard, 2000;McGlashan et al, 2015;Taylor et al, 2014) and in contrast to the relatively constant f H during incubation of Squamata (Birchard and Reiber, 1996;Nechaeva et al, 2007;Du et al, 2009;Sartori et al, 2017). In snapping turtles, f H reduction has been related to the onset of parasympathetic tone, which is present at 70% incubation (Alvine et al, 2013), in comparison to the late onset of vagal tone found in green iguana (Sartori et al, 2015) and the lack of vagal tone during incubation in the American alligator (Eme et al, 2011).…”

“…To support this growth, egg VȮ 2 doubled during the last half of the incubation period but f H decreased by 23%, which resulted in a 3-fold increase in O 2 pulse. Our previous study in a squamate reptile showed that VȮ 2 varied independently of f H (Sartori et al, 2017), indicating that other physiological mechanisms were involved in matching O 2 supply to tissue demand during embryonic incubation. In the present study, heart mass tripled from 50% to 90% incubation (Table 1) and this was coupled to an increase in oxygen pulse (Fig.…”

“…Egg oxygen consumption increases with development as the mass of embryonic tissues increases due to growth and differentiation (Thompson, 1989;Booth, 1998a,b;Booth et al, 2000;Crossley et al, 2017a) and the convective oxygen transport system must be sufficient to supply this demand. While the components of oxygen delivery have not been extensively investigated in developing animals, metabolic rate has been studied in numerous species representing all reptilian lineages (Lynn and Von Brand, 1945;Dmi'el, 1970;Ackerman, 1981;Thompson, 1989;Booth and Thompson, 1991;Whitehead and Seymour, 1990;Thompson, 1993;Aulie and Kanui, 1995;Birchard and Reiber, 1995;Thompson and Stewart, 1997;Booth, 1998a,b;Vleck and Hoyt, 1991;Russell, 1998, 1999;Booth et al, 2000;Sartori et al, 2017;Crossley et al, 2017a). The patterns of whole-egg metabolism in many species are characterized as peaking at some point prior to hatching followed by either a plateau or a decrease (Gettinger et al, 1984;Thompson, 1989;Miller and Packard, 1992;Booth, 1998a,b;Booth et al, 2000;Crossley et al, 2017a).…”