Aquatic surface respiration and swimming behaviour in adult and developing zebrafish exposed to hypoxia

Abstract

Severe hypoxia elicits aquatic surface respiration (ASR) behaviour in many species of fish, where ventilation of the gills at the air-water interface improves O 2 uptake and survival. ASR is an important adaptation that may have given rise to air breathing in vertebrates. The neural substrate of this behaviour, however, is not defined. We characterized ASR in developing and adult zebrafish (Danio rerio) to ascertain a potential role for peripheral chemoreceptors in initiation or modulation of this response. Adult zebrafish exposed to acute, progressive hypoxia (P O2 from 158 to 15 mmHg) performed ASR with a threshold of 30 mmHg, and spent more time at the surface as P O2 decreased. Acclimation to hypoxia attenuated ASR responses. In larvae, ASR behaviour was observed between 5 and 21 days postfertilization with a threshold of 16 mmHg. Zebrafish decreased swimming behaviour (i.e. distance, velocity and acceleration) as P O2 was decreased, with a secondary increase in behaviour near or below threshold P O2 . In adults that underwent a 10-day intraperitoneal injection regime of 10 μg g −1 serotonin (5-HT) or 20 μg g −1 acetylcholine (ACh), an acute bout of hypoxia (15 mmHg) increased the time engaged in ASR by 5.5 and 4.9 times, respectively, compared with controls. Larvae previously immersed in 10 μmol l −1 5-HT or ACh also displayed an increased ASR response. Our results support the notion that ASR is a behavioural response that is reliant upon input from peripheral O 2 chemoreceptors. We discuss implications for the role of chemoreceptors in the evolution of air breathing.

IgG-Containing Isoforms of Neuregulin-1 Are Dispensable for Cardiac Trabeculation in Zebrafish

“…Unlike mammalian models, zebrafish embryos are small enough to meet oxygen needs by diffusion alone and can survive for days with severe heart malformations [24–28]. Further, adult zebrafish are highly tolerant of reduced cardiac function [29,30]. …”

Regulation of erythrocyte function: Multiple evolutionary solutions for respiratory gas transport and its regulation in fish

“…5 Three major alternative solutions in the gas transport by erythrocytes have evolved in fish: that employed by agnathans, 6 that used by elasmobranchs, 7,8 and that found in teleosts. [13][14][15] Although direct link to gas transport cannot be yet made, it is of interest that different from mammals all zebrafish cells exhibit circadian rhythm. 10 Apart from mammals, all vertebrates have erythrocytes that are nucleated and contain other cell organelles, which may partly explain why many features of the regulation of erythrocyte function, important for the different environmental adaptations in fish, are not utilized in air-breathing mammals with their organelle-free erythrocytes.…”

Cardiorespiratory physiological phenotypic plasticity in developing air‐breathing anabantid fishes ( Betta splendens and Trichopodus trichopterus )

“…Acute hypoxic exposure in aquatic fishes triggers reflex responses aimed at maintaining homeostasis, including reflex branchial hyperventilation – for reviews see (Abdallah et al. ; Martin ; Milsom ; Perry ; Porteus et al. ).…”

“…Air breathing may be a response to nocturnal or seasonal hypoxia in so‐called “facultative” air‐breathing fishes, or may be required in “obligatory” air breathers – for reviews, see (Abdallah et al. ; Burggren ; Burggren and Johansen ; Johansen and Lenfant ; Martin ; Milsom ; Perry ; Porteus et al. ).…”

“…Acute hypoxic exposure in aquatic fishes triggers reflex responses aimed at maintaining homeostasis, including reflex branchial hyperventilationfor reviews see (Abdallah et al 2015;Martin 2014;Milsom 2012;Perry 2011;Porteus et al 2011). Frequently 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).…”