Heart rate during development in the turtle embryo: effect of temperature

SUMMARYThe eggs of birds typically hatch after a fixed (but lineage-specific) cumulative number of heart beats since the initiation of incubation. Is the same true for non-avian reptiles, despite wide intraspecific variation in incubation period generated by variable nest temperatures? Non-invasive monitoring of embryo heart beat rates in one turtle species (Pelodiscus sinensis) and two lizards (Bassiana duperreyi and Takydromus septentrionalis) show that the total number of heart beats during embryogenesis is relatively constant over a wide range of warm incubation conditions. However, incubation at low temperatures increases the total number of heart beats required to complete embryogenesis, because the embryo spends much of its time at temperatures that require maintenance functions but that do not allow embryonic growth or differentiation. Thus, cool-incubated embryos allocate additional metabolic effort to maintenance costs. Under warm conditions, total number of heart beats thus predicts incubation period in non-avian reptiles as well as in birds (the total number of heart beats are also similar); however, under the colder nest conditions often experienced by non-avian reptiles, maintenance costs add significantly to total embryonic metabolic expenditure.

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Determinants of incubation period: do reptilian embryos hatch after a fixed total number of heart beats?

Radder

Sun

et al. 2009

“…5). f H fell slightly before and markedly after hatching in the snapping turtle, Chelydra serpentina, indicating the establishment of an effective vagal tonus on the heart, coincident with the onset of lung breathing (Birchard and Reiber, 1996). A number of turtles and tortoises lack cholinergic tone on f H until the time of hatching although cholinergic tonus was verified during the final 30% of embryonic incubation in snapping turtles (Alvine et al, 2013) (Fig.…”

Section: Reviewmentioning

confidence: 92%

“…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.…”

Section: Reviewmentioning

confidence: 99%

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

Taylor

Leite

Sartori

et al. 2014

Heart rate in vertebrates is controlled by activity in the autonomic nervous system. In spontaneously active or experimentally prepared animals, inhibitory parasympathetic control is predominant and is responsible for instantaneous changes in heart rate, such as occur at the first air breath following a period of apnoea in discontinuous breathers like inactive reptiles or species that surface to air breathe after a period of submersion. Parasympathetic control, exerted via fast-conducting, myelinated efferent fibres in the vagus nerve, is also responsible for beat-to-beat changes in heart rate such as the high frequency components observed in spectral analysis of heart rate variability. These include respiratory modulation of the heartbeat that can generate cardiorespiratory synchrony in fish and respiratory sinus arrhythmia in mammals. Both may increase the effectiveness of respiratory gas exchange. Although the central interactions generating respiratory modulation of the heartbeat seem to be highly conserved through vertebrate phylogeny, they are different in kind and location, and in most species are as yet little understood. The heart in vertebrate embryos possesses both muscarinic cholinergic and β-adrenergic receptors very early in development. Adrenergic control by circulating catecholamines seems important throughout development. However, innervation of the cardiac receptors is delayed and first evidence of a functional cholinergic tonus on the heart, exerted via the vagus nerve, is often seen shortly before or immediately after hatching or birth, suggesting that it may be coordinated with the onset of central respiratory rhythmicity and subsequent breathing.

“…a Q 10 effect) and induces thermal acclimation of heart rate (i.e. changes in Q 10 ) (Birchard and Reiber, 1996;Birchard, 2000;Du et al, 2010). Temperature-induced variation (or sex differences) in heart rate (f H ) and arterial blood pressure (P m ) could influence growth and metabolism through changes in tissue perfusion, gas exchange and nutrient/waste transport.…”

Section: Introductionmentioning

confidence: 99%

Temperature-dependent sex determination modulates cardiovascular maturation in embryonic snapping turtles, Chelydra serpentina

Alvine

Rhen

Crossley

2012

SUMMARYWe investigated sex differences in cardiovascular maturation in embryos of the snapping turtle Chelydra serpentina, a species with temperature-dependent sex determination. One group of eggs was incubated at 26.5°C to produce males. Another group of eggs was incubated at 26.5°C until embryos reached stage 17; eggs were then shifted to 31°C for 6days to produce females, and returned to 26.5°C for the rest of embryogenesis. Thus, males and females were at the same temperature when autonomic tone was determined and for most of development. Cholinergic blockade increased resting blood pressure (P m ) and heart rate (f H ) in both sexes at 75% and 90% of incubation. However, the magnitude of the f H response was enhanced in males compared with females at 90% of incubation. β-adrenergic blockade increased P m at 75% of incubation in both sexes but had no effect at 90% of incubation. β-adrenergic blockade reduced f H at both time points but produced a stronger response at 90% versus 75% of incubation. We found that α-adrenergic blockade decreased P m in both sexes at 75% and 90% of incubation and decreased f H at 75% of incubation in both sexes. At 90% of incubation, f H decreased in females but not males. Although these data clearly demonstrate sexual dimorphism in the autonomic regulation of cardiovascular physiology in embryos, further studies are needed to test whether differences are caused by endocrine signals from gonads or by a hormone-independent temperature effect.