Reptile embryos tolerate large decreases in the concentration of ambient oxygen. However, we do not fully understand the mechanisms that underlie embryonic cardiovascular short- or long-term responses to hypoxia in most species. We therefore measured cardiac growth and function in snapping turtle embryos incubated under normoxic (N21; 21% O₂) or chronic hypoxic conditions (H10; 10% O₂). We determined heart rate (fH) and mean arterial pressure (Pm) in acute normoxic (21% O₂) and acute hypoxic (10% O₂) conditions, as well as embryonic responses to cholinergic, adrenergic, and ganglionic pharmacological blockade. Compared with N21 embryos, chronic H10 embryos had smaller bodies and relatively larger hearts and were hypotensive, tachycardic, and following autonomic neural blockade showed reduced intrinsic fH at 90% of incubation. Unlike other reptile embryos, cholinergic and ganglionic receptor blockade both increased fH. β-Adrenergic receptor blockade with propranolol decreased fH, and α-adrenergic blockade with phentolamine decreased Pm. We also measured cardiac mRNA expression. Cholinergic tone was reduced in H10 embryos, but cholinergic receptor (Chrm2) mRNA levels were unchanged. However, expression of adrenergic receptor mRNA (Adrb1, Adra1a, Adra2c) and growth factor mRNA (Igf1, Igf2, Igf2r, Pdgfb) was lowered in H10 embryos. Hypoxia altered the balance between cholinergic receptors, α-adrenoreceptor and β-adrenoreceptor function, which was reflected in altered intrinsic fH and adrenergic receptor mRNA levels. This is the first study to link gene expression with morphological and cardioregulatory plasticity in a developing reptile embryo.
Embryonic alligator responses to adrenergic blockade with propranolol and phentolamine were very similar to previously reported responses of embryonic chicken, and demonstrated that embryonic alligator have α and β-adrenergic tone over the final third of development. However, adrenergic tone originates entirely from circulating catecholamines and is not altered by chronic hypoxic incubation, as neither cholinergic blockade with atropine nor ganglionic blockade with hexamethonium altered baseline cardiovascular variables in N21 or H10 embryos. In addition, both atropine and hexamethonium injection did not alter the generally depressive effects of acute hypoxia -bradycardia and hypotension. However, H10 embryos showed significantly higher levels of noradrenaline and adrenaline at 70% of development, as well as higher noradrenaline at 80% of development, suggesting that circulating catecholamines reach maximal levels earlier in incubation for H10 embryos, compared to N21 embryos. Chronically elevated levels of catecholamines may alter the normal balance between α and β-adrenoreceptors in H10 alligator embryos, causing chronic bradycardia and hypotension of H10 embryos measured in normoxia.
The timing, success and energetics of fish embryonic development are strongly influenced by temperature. However, it is unclear if there are developmental periods, or critical windows, when oxygen use, survival and hatchling phenotypic characteristics are particularly influenced by changes in the thermal environment. Therefore, we examined the effects of constant incubation temperature and thermal shifts on survival, hatchling phenotype, and cost of development in lake whitefish (Coregonus clupeaformis) embryos. We incubated whitefish embryos at control temperatures of 2, 5, or 8 °C, and shifted embryos across these three temperatures at the end of gastrulation or organogenesis. We assessed hatch timing, mass at hatch, and yolk conversion efficiency (YCE). We determined cost of development, the amount of oxygen required to build a unit of mass, for the periods from fertilization-organogenesis, organogenesis-fin flutter, fin flutter-hatch, and for total development. An increase in incubation temperature decreased time to 50 % hatch (164 days at 2 °C, 104 days at 5 °C, and 63 days at 8 °C), survival decreased from 55 % at 2 °C, to 38 % at 5 °C, and 17 % at 8 °C, and hatchling yolk-free dry mass decreased from 1.27 mg at 2 °C to 0.61 mg at 8 °C. Thermal shifts altered time to 50 % hatch and hatchling yolk-free dry mass and revealed a critical window during gastrulation in which a temperature change reduced survival. YCE decreased and cost of development increased with increased incubation temperature, but embryos that hatched at 8 °C and were incubated at colder temperatures during fertilization-organogenesis had reduced cost. The relationship between cost of development and temperature was altered during fin flutter-hatch, indicating it may be a critical window during which temperature has the greatest impact on energetic processes. The increase in cost of development with an increase in temperature has not been documented in other fishes and suggests whitefish embryos are more energy efficient at colder temperatures.
Environmental conditions fluctuate dramatically in some reptilian nests. However, critical windows of environmental sensitivity for cardiovascular development have not been identified. Continuous developmental hypoxia has been shown to alter cardiovascular form and function in embryonic snapping turtles (Chelydra serpentina), and we used this species to identify critical periods during which hypoxia modifies the cardiovascular phenotype. We hypothesized that incubation in 10% O2 during specific developmental periods would have differential effects on the cardiovascular system versus overall somatic growth. Two critical windows were identified with 10% O2 from 50% to 70% of incubation, resulting in relative heart enlargement, either via preservation of or preferential growth of this tissue, while exposure to 10% O2 from 20% to 70% of incubation resulted in a reduction in arterial pressure. The deleterious or advantageous aspects of these embryonic phenotypes in posthatching snapping turtles have yet to be explored. However, identification of these critical windows has provided insight into how the developmental environment alters the phenotype of reptiles and will also be pivotal in understanding its impact on the fitness of egg-laying reptiles.
The considerable quantities of dead wood in the intertidal zone of mature mangrove forests are tunnelled by bivalves of the family Teredinidae. When the surface of heavily tunnelled wood is broken open, cryptofauna are able to use tunnels as refuges. In this study, the exploitation of this niche during low tide by the dartfish Parioglossus interruptus was investigated. The majority of tunnels offer a close fit falling within the range of typical dartfish diameters. The fish found within wood tended to be smaller than fish found swimming between mangrove roots at high tide. Dartfish were found in tunnelled wood even where it was emersed for over 11 h d −1 , but favoured wood in the lower intertidal. Within the wood, daytime thermal maxima were reduced by 6.5°C compared with adjacent tidepools. Wind-tunnel observations indicated that this lowering could be due to evaporative cooling. However, dartfish were found to be notably tolerant of high temperatures, with a critical thermal maximum that exceeded temperatures reached in tunnelled wood and pools. Nonetheless, such tolerance may impose a metabolic cost that would be reduced by occupying tunnels. Teredinid tunnels are also likely to give dartfish protection from desiccation and predation. During high-tide, free-swimming dartfish were observed to favour areas of Rhizophora roots over open creeks. In aquaria, fish swam actively during the day, but took refuge in teredinid tunnels at night. Sampling of wood at low tide and direct observations at high tide indicate that a substantial proportion of the dartfish population takes refuge in wood during low tide. Thus, teredinid-tunnelled wood is a key low-tide refuge especially for younger fish, which would otherwise be exposed to predators. This study provides an example of a mechanism whereby mangrove forests support intertidal biodiversity.
This review explores challenges and opportunities in developmental physiology outlined by a symposium at the 2014 American Physiological Society Intersociety Meeting: Comparative Approaches to Grand Challenges in Physiology. Across animal taxa, adverse embryonic/fetal environmental conditions can alter morphological and physiological phenotypes in juveniles or adults, and capacities for developmental plasticity are common phenomena. Human neonates with body sizes at the extremes of perinatal growth are at an increased risk of adult disease, particularly hypertension and cardiovascular disease. There are many rewarding areas of current and future research in comparative developmental physiology. We present key mechanisms, models, and experimental designs that can be used across taxa to investigate patterns in, and implications of, the development of animal phenotypes. Intraspecific variation in the timing of developmental events can be increased through developmental plasticity (heterokairy), and could provide the raw material for selection to produce heterochrony — an evolutionary change in the timing of developmental events. Epigenetics and critical windows research recognizes that in ovo or fetal development represent a vulnerable period in the life history of an animal, when the developing organism may be unable to actively mitigate environmental perturbations. ‘Critical windows’ are periods of susceptibility or vulnerability to environmental or maternal challenges, periods when recovery from challenge is possible, and periods when the phenotype or epigenome has been altered. Developmental plasticity may allow survival in an altered environment, but it also has possible long-term consequences for the animal. “Catch-up growth” in humans after the critical perinatal window has closed elicits adult obesity and exacerbates a programmed hypertensive phenotype (one of many examples of “fetal programing”). Grand challenges for developmental physiology include integrating variation in developmental timing within and across generations, applying multiple stressor dosages and stressor exposure at different developmental timepoints, assessment of epigenetic and parental influences, developing new animal models and techniques, and assessing and implementing these designs and models in human health and development.
All crocodilians have complete anatomical separation between the right and left ventricles, which is similar to birds and mammals and unlike all other non-avian reptiles. However, the crocodilian heart retains two systemic aortae (left aorta and right aortic arch), a feature that is common to all non-avian reptiles. In crocodilians, the left aorta (LAo) emerges from the right ventricle (RV) alongside the pulmonary artery (PA), and the right aortic arch (RAo) emerges from the left ventricle (LV) (Webb, 1979). This anatomical arrangement results in the capacity for a 'right-to-left' (R-L) cardiac shunt, a 'pulmonary bypass' cardiac shunt, in which a fraction of systemic venous blood recirculates into the systemic arterial circulation (Hicks, 1998).The crocodilian RAo and LAo communicate at two distinct points. As the aortae emerge from the heart, they run side-by-side, sharing a common wall for several centimetres. Near the base of this common wall and just downstream of the aortic valves, there is a small opening called the foramen of Panizza (FoP) (Panizza, 1833), which is of variable calibre and allows for potential blood flow between the RAo and LAo (Grigg and Johansen, 1987;Axelsson et al., 1996;Axelsson and Franklin, 2001). The second point of communication between the aortae is an arterial anastomosis in the abdominal cavity, caudal to the liver. Beyond this anastomosis, the RAo continues as the dorsal aortal, and the LAo becomes the coeliac artery, which gives rise to smaller arteries that supply most of the blood flow to the gastrointestinal tract. Consequently, the LAo is the primary source of blood for the splanchnic circulation, although blood from the RAo can also enter the splanchnic bed via the anastomosis (Axelsson et al., 1991).R-L cardiac shunt has been hypothesised to be important in various activities and physiological functions (Hicks, 1998;Hicks, 2002). For semi-aquatic reptiles like crocodilians, generation of a R-L cardiac shunt has often been observed during breath-holds associated with diving (White, 1969;Grigg and Johansen, 1987;Hicks and Wang, 1996). The reduction in pulmonary blood flow during apnoea has been hypothesised to conserve lung O 2 stores and sequester CO 2 away from the lung, possibly extending aerobic dive times (White, 1978;White, 1985;Grigg and Johansen, 1987). The development of a R-L cardiac shunt also results in arterial desaturation through admixture of venous blood, and the resulting systemic hypoxemia can trigger tissue hypometabolism, which could contribute to the prolongation of aerobic dives (Hicks and Wang, 1999;Platzack and Hicks, 2001).Crocodilians provide an opportunity to investigate experimentally the proximate functions of reptilian cardiac shunting. Their cardiac anatomy lends itself to surgical modification that prevents R-L cardiac shunt while maintaining the integrity of the ventricular chambers, a procedure that is not possible in other reptiles. The purpose of the present study was to test the hypotheses that removal of shunt (occlusion of LAo) woul...
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
334 Leonard St
Brooklyn, NY 11211
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.