Cardiovascular development in embryos of the American alligator <i>Alligator mississippiensis</i>: effects of chronic and acute hypoxia

Crossley, Dane A.; Altimiras, Jordi

doi:10.1242/jeb.01355

Cited by 86 publications

(120 citation statements)

References 33 publications

(51 reference statements)

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“…6). Alligator embryos also lack central nervous control of f H in response to hypoxia and exhibit a limited hypertensive baroreflex response (Crossley et al, 2003a;Crossley and Altimiras, 2005). We have recently obtained similar findings in the Paraguayan caiman (D.A.C., unpublished) (Fig.…”

Section: Reviewsupporting

confidence: 67%

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

Taylor

Leite

Sartori

et al. 2014

Journal of Experimental Biology

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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.

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Section: Reviewsupporting

confidence: 67%

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

Taylor

Leite

Sartori

et al. 2014

Journal of Experimental Biology

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“…Chronic hypoxia during embryonic development has a profound effect on reptiles, changing the trajectory of phenotype maturation of multiple systems, with a pronounced impact on the cardiovascular system (Kam, 1993;Crossley et al, 2003;Crossley and Altimiras, 2005;Owerkowicz et al, 2009;Eme et al, 2011Eme et al, , 2013Eme et al, , 2014Enok et al, 2013;Tate et al, 2015Tate et al, , 2016Wearing et al, 2016). Over the past decade, our understanding of embryonic cardiovascular development in these species has improved markedly.…”

Section: Introductionmentioning

confidence: 99%

“…However, very few studies have determined lasting impacts of morphological and physiological phenotypic modifications on juveniles and adults (Owerkowicz et al, 2009;Galli et al, 2016;Wearing et al, 2016). Much of the work that has been conducted so far has illustrated that embryonic reductions in oxygen availability restrict body mass at hatching (Kam, 1993;Crossley and Altimiras, 2005;Owerkowicz et al, 2009;Eme et al, 2011Eme et al, , 2013Eme et al, , 2014Marks et al, 2013;Tate et al, 2015Tate et al, , 2016Crossley et al, 2017b), and this persists into the first years of posthatching life (Owerkowicz et al, 2009;Galli et al, 2016;Wearing et al, 2016). In addition, heart mass is relatively enlarged in embryonic reptiles chronically exposed to low oxygen (Kam, 1993;Crossley and Altimiras, 2005;Eme et al, 2013Eme et al, , 2014Marks et al, 2013;Tate et al, 2015Tate et al, , 2016, which again persists at least into the first years after hatching in American alligators (Owerkowicz et al, 2009;Galli et al, 2016), indicating that developmental hypoxia has a lasting impact on the cardiovascular phenotype of this species.…”

Section: Introductionmentioning

confidence: 99%

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

Wearing

Conner

Nelson

et al. 2017

Journal of Experimental Biology

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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.

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“…In contrast, hypoxia reduces the heart rate of American alligators [Alligator mississippiensis (Daudin, 1802)] (Crossley & Altimiras 2005a) and some species of birds (VanGolde et al 1997). In addition, other mechanisms such as an enlarged heart (Snyder et al 1982;Kam 1993;Crossley & Altimiras 2005b), region-specific changes in vascular density on the chorioallantoic membrane, increases in hematocrit and an acceleration and redistribution of blood flow have been demonstrated to increase O 2 transport rates under hypoxic conditions (Kam 1993;Warburton et al 1995;VanGolde et al 1997;Corona & Warburton 2000). Further studies on these aspects would be of great interest and important to our understanding of the physiological responses of amniote embryos to hypoxia.…”

Section: Figurementioning

confidence: 99%

Reduced egg shell permeability affects embryonic development and hatchling traits in Lycodon rufozonatum and Pelodiscus sinensis

Tang

Chen

2018

Integrative Zoology

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The response of embryos to unpredictable hypoxia is critical for successful embryonic development, yet there remain significant gaps in our understanding of such responses in reptiles with different types of egg shell. We experimentally generated external regional hypoxia by sealing either the upper half or bottom half of the surface area of eggs in 2 species of reptiles (snake [Lycodon rufozonatum] with parchment egg shell and Chinese softshelled turtle [Pelodiscus sinensis] with rigid egg shell), then monitored the growth pattern of the opaque white patch in turtle eggs (a membrane that attaches the embryo to the egg shell and plays an important role in gas exchange), the embryonic heart rate, the developmental rate and the hatchling traits in turtle and snake eggs in response to external regional hypoxia. The snake embryos from the hypoxia treatments facultatively increased their heart rate during incubation, and turtle embryos from the upper-half hypoxia treatment enhanced their growth of the opaque white patch. Furthermore, the incubation period and hatching success of embryos were not affected by the hypoxia treatment in these 2 species. External regional hypoxia significantly affected embryonic yolk utilization and offspring size in the snake and turtle. Compared to sham controls, embryos from the upper-half hypoxia treatment used less energy from yolk and, therefore, developed into smaller hatchlings, but embryos from the bottom-half hypoxia treatment did not.

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Cardiovascular development in embryos of the American alligator Alligator mississippiensis: effects of chronic and acute hypoxia

Cited by 86 publications

References 33 publications

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

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

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

Reduced egg shell permeability affects embryonic development and hatchling traits in Lycodon rufozonatum and Pelodiscus sinensis

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