Abstract

Developmental plasticity of cardiorespiratory physiology in response to chronic hypoxia is poorly understood in larval fishes, especially larval air‐breathing fishes, which eventually in their development can at least partially “escape” hypoxia through air breathing. Whether the development air breathing makes these larval fishes less or more developmentally plastic than strictly water breathing larval fishes remains unknown. Consequently, developmental plasticity of cardiorespiratory physiology was determined in two air‐breathing anabantid fishes (Betta splendens and Trichopodus trichopterus). Larvae of both species experienced an hypoxic exposure that mimicked their natural environmental conditions, namely chronic nocturnal hypoxia (12 h at 17 kPa or 14 kPa), with a daily return to diurnal normoxia. Chronic hypoxic exposures were made from hatching through 35 days postfertilization, and opercular and heart rates measured as development progressed. Opercular and heart rates in normoxia were not affected by chronic nocturnal hypoxic. However, routine oxygen consumption M˙O2 (~4 μmol·O2/g per hour in normoxia in larval Betta) was significantly elevated by chronic nocturnal hypoxia at 17 kPa but not by more severe (14 kPa) nocturnal hypoxia. Routine M˙O2 in Trichopodus (6–7 μmol·O2/g per hour), significantly higher than in Betta, was unaffected by either level of chronic hypoxia. P Crit, the PO2 at which M˙O2 decreases as ambient PO2 falls, was measured at 35 dpf, and decreased with increasing chronic hypoxia in Betta, indicating a large, relatively plastic hypoxic tolerance. However, in contrast, P Crit in Trichopodus increased as rearing conditions grew more hypoxic, suggesting that hypoxic acclimation led to lowered hypoxic resistance. Species‐specific differences in larval physiological developmental plasticity thus emerge between the relatively closely related Betta and Trichopodus. Hypoxic rearing increased hypoxic tolerance in Betta, which inhabits temporary ponds with nocturnal hypoxia. Trichopodus, inhabiting more permanent oxygenated bodies of water, showed few responses to hypoxia, reflecting a lower degree of developmental phenotypic plasticity.

Highlights

  • Acute hypoxic exposure in aquatic fishes triggers reflex responses aimed at maintaining homeostasis, including reflex branchial hyperventilation – for reviews see (Abdallah et al 2015; Martin 2014; Milsom 2012; Perry 2011; Porteus et al 2011)

  • Physiological Reports published by Wiley Periodicals, Inc. on behalf of The Physiological Society and the American Physiological Society

  • (2) Chronic hypoxia: Rearing in chronic hypoxia did not induce any significant changes in gill ventilation measured in normoxia in larval Betta (F = 7, df = 6, 63, and P > 0.05) (Fig. 1A)

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Summary

Introduction

Acute hypoxic exposure in aquatic fishes triggers reflex responses aimed at maintaining homeostasis, including reflex branchial hyperventilation – for reviews see (Abdallah et al 2015; Martin 2014; Milsom 2012; Perry 2011; Porteus et al 2011). Concurrent with hypoxia-induced increases in gill ventilation is a reflex bradycardia, and increases in stroke volume and branchial vascular resistance (Farrell 2007; Gamperl and Driedzic 2009; Gamperl and Farrell 2004; Pelster 1999; Stecyk et al 2008; Tota et al 2011; Wilson et al 2015) These physiological and behavioral responses to aquatic hypoxia in fishes – collectively representing the hypoxic ventilatory a 2017 The Authors. Burggren reflex – are often accompanied by numerous other additional physiological adjustments, including changes in hemoglobin oxygen binding affinity, blood O2 carrying capacity, stroke volume, and branchial vascular resistance All these adjustments to hypoxia can contribute to enhanced O2 transfer and potentially lowered ventilatory convection requirement (Gamperl and Driedzic 2009; Perry et al 2009). As aquatic PO2 falls, the high cost of gill ventilation with water may become prohibitive, especially when combined with failure of adequate tissue oxygen transport associated with low arterial PO2 (Diaz and Breitburg 2009; Farrell and Richards 2009; Graham 1997; Randall et al 1981)

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