Abstract
Hypoxia during embryonic growth in embryos is frequently a powerful determinant of development, but at least in avian embryos the effects appear to show considerable intra- and inter-specific variation. We hypothesized that some of this variation may arise from different protocols that may or may not result in exposure during the embryo’s critical window for hypoxic effects. To test this hypothesis, quail embryos (Coturnix coturnix) in the intact egg were exposed to hypoxia (~15% O2) during “early” (Day 0 through Day 5, abbreviated as D0-D5), “middle” (D6-D10) or “late” (D11-D15) incubation or for their entire 16–18 day incubation (“continuous hypoxia”) to determine critical windows for viability and growth. Viability, body mass, beak and toe length, heart mass, and hematology (hematocrit and hemoglobin concentration) were measured on D5, D10, D15 and at hatching typically between D16 and D18 Viability rate was ~50–70% immediately following the exposure period in the early, middle and late hypoxic groups, but viability improved in the early and late groups once normoxia was restored. Middle hypoxia groups showed continuing low viability, suggesting a critical period from D6-D10 for embryo viability. The continuous hypoxia group experienced viability reaching <10% after D15. Hypoxia, especially during late and continuous hypoxia, also inhibited growth of body, beak and toe when measured at D15. Full recovery to normal body mass upon hatching occurred in all other groups except for continuous hypoxia. Contrary to previous avian studies, heart mass, hematocrit and hemoglobin concentration were not altered by any hypoxic incubation pattern. Although hypoxia can inhibit embryo viability and organ growth during most incubation periods, the greatest effects result from continuous or middle incubation hypoxic exposure. Hypoxic inhibition of growth can subsequently be “repaired” by catch-up growth if a final period of normoxic development is available. Collectively, these data indicate a critical developmental window for hypoxia susceptibility during the mid-embryonic period of development.
Highlights
Normal morphological and physiological development of the avian embryo, as well as successful hatching, depends on appropriate temperature as well as ambient partial pressures of oxygen, carbon dioxide, and water vapor–for an entry into the voluminous, long-standing literature see [1,2]
Studies of critical windows in chicken embryos have investigated for sensitivity to hypoxia for control of ventilation [34], for metabolic rate [25] and for morphological characteristics including craniofacial shape [35]
Specific critical windows across the entire span of embryonic development, when organogenesis, tissue differentiation and growth may be vulnerable to hypoxia, have not been comprehensively investigated
Summary
Normal morphological and physiological development of the avian embryo, as well as successful hatching, depends on appropriate temperature as well as ambient partial pressures of oxygen, carbon dioxide, and water vapor–for an entry into the voluminous, long-standing literature see [1,2]. Embryonic responses–both adaptive and maladaptive—to hypoxic incubation in avian embryos include (but are not limited to) whole body growth retardation, reduction in oxygen consumption, specific growth retardation of organs like the beak and toes, heart hypertrophy, changes in heart conduction and cardiac rhythms, pericardial and pulmonary edema, accelerated angiogenesis, stimulated hematopoesis, hemoglobin modifications (including changes in the time course of adult Hb appearance) and red blood cell ATP concentration changes [3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28] Most of these studies on the effect of hypoxia on avian development have exposed embryos to chronic hypoxia throughout the entire incubation prior to measurements or during the last half of incubation—see [6] for discussion of the most common hypoxic exposure protocols. We hypothesized that the first third of avian incubation would prove to be the most sensitive to hypoxic exposure, based on experiments on hypoxic viability in chicken embryos cited above
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