Effects of aerial hypoxia and temperature on pulmonary breathing pattern and gas exchange in the South American lungfish, Lepidosiren paradoxa

Abstract

The South American lungfish Lepidosiren paradoxa is an obligatory air-breathing fish possessing well-developed bilateral lungs, and undergoing seasonal changes in its habitat, including temperature changes. In the present study we aimed to evaluate gas exchange and pulmonary breathing pattern in L. paradoxa at different temperatures (25 and 30°C) and different inspired O levels (21, 12, 10, and 7%). Normoxic breathing pattern consisted of isolated ventilatory cycles composed of an expiration followed by 2.4±0.2 buccal inspirations. Both expiratory and inspiratory tidal volumes reached a maximum of about 35mlkg, indicating that L. paradoxa is able to exchange nearly all of its lung air in a single ventilatory cycle. At both temperatures, hypoxia caused a significant increase in pulmonary ventilation (V̇), mainly due to an increase in respiratory frequency. Durations of the ventilatory cycle and expiratory and inspiratory tidal volumes were not significantly affected by hypoxia. Expiratory time (but not inspiratory) was significantly shorter at 30°C and at all O levels. While a small change in oxygen consumption (V̇O) could be noticed, the carbon dioxide release (V̇CO, P=0.0003) and air convection requirement (V̇/V̇O, P=0.0001) were significantly affected by hypoxia (7% O) at both temperatures, when compared to normoxia, and pulmonary diffusion capacity increased about four-fold due to hypoxic exposure. These data highlight important features of the respiratory system of L. paradoxa, capable of matching O demand and supply under different environmental change, as well as help to understand the evolution of air breathing in lungfish.

Social dynamics obscure the effect of temperature on air breathing in Corydoras catfish

“…Overall, groups had a higher ABF after the 2 week acclimation to 30°C, especially at 20% oxygen availability. This may be due to hypoxia being exacerbated at higher temperatures due to a reduction in dissolved oxygen or elevated metabolic rate, which may have increased oxygen demand ( Breitburg et al, 2018 ; da Silva et al, 2017 ; Graham, 1997 ). Wang and Lin (2018) compared ABF under hypoxia alone, temperature alone, and then both stressors combined and found that ABF was highest at the most extreme temperature and hypoxia combination.…”

Control of air-breathing in fishes: Central and peripheral receptors

“…An increase in temperature is a combined systemic/environmental factor that stimulates air-breathing behavior in fishes because it increases the demand for O 2 in the tissues and requires increased O 2 delivery (Johansen et al, 1970;Rahn et al, 1971;Horn and Riggs, 1973;Graham and Baird, 1982;Glass et al, 1986;Johnston and Dunn, 1987;McMahon and Burggren, 1987;Smatresk, 1988;Clarke and Johnston, 1999;Geiger et al, 2000;Silva et al, 2017). Indeed, warming also lowers O 2 solubility in water, which reduces aquatic P O2 and additionally contributes to stimulate air-breathing behavior (Rahn, 1966;Johansen et al, 1970;Graham and Baird, 1982;McMahon and Burggren, 1987).…”

“…Electrophorus electricus exhibits no change in air-breathing frequency during aquatic hypoxia while Trichogaster trichopterus exhibits an increase) but not among sarcopterygians (aquatic hypoxia does not change air-breathing frequency in Lepidosiren paradoxa, Protopterus aethiopicus and Protopterus dolloi) Sanchez et al, 2001a;Perry et al, 2005a). It is conceivable that obligate sarcopterygians do not possess externally oriented O 2 chemoreceptors in the gills (Lahiri et al, 1970;Perry et al, 2005a;Silva et al, 2017). However, the actinopterygian and sarcopterygian species just cited, as well as the obligate air-breathing teleosts C. argus and Monopterus cuchia, show an increase in air-breathing frequency when exposed to aerial hypoxia, which may have been triggered by hypoxaemia through internally oriented chemoreceptors or by external chemoreceptors that monitor the P O2 of air in the ABO Lomholt and Johansen, 1974;Glass et al, 1986;Sanchez et al, 2001a;Zaccone et al, 2003Zaccone et al, , 2006Perry et al, 2005a;Silva et al, 2011Silva et al, , 2017.…”

“…It is conceivable that obligate sarcopterygians do not possess externally oriented O 2 chemoreceptors in the gills (Lahiri et al, 1970;Perry et al, 2005a;Silva et al, 2017). However, the actinopterygian and sarcopterygian species just cited, as well as the obligate air-breathing teleosts C. argus and Monopterus cuchia, show an increase in air-breathing frequency when exposed to aerial hypoxia, which may have been triggered by hypoxaemia through internally oriented chemoreceptors or by external chemoreceptors that monitor the P O2 of air in the ABO Lomholt and Johansen, 1974;Glass et al, 1986;Sanchez et al, 2001a;Zaccone et al, 2003Zaccone et al, , 2006Perry et al, 2005a;Silva et al, 2011Silva et al, , 2017. Nonetheless, the facultative sarcopterygian N. forsteri did not exhibit this response after the injection of nitrogen into the lung .…”

“…Regarding sarcopterygians, there is one report that external nicotine injections stimulate air-breathing in the African lungfish (P. aethiopicus) , but such kind of external stimuli has more often failed to trigger this behavior in dipnoans Sanchez et al, 2001a;Perry et al, 2005a). On the other hand, internal NaCN injections triggered air-breathing responses in P. aethiopicus (Lahiri et al, 1970), as well as exposure to aerial hypoxia did in L. paradoxa, P. aethiopicus and P. dolloi Sanchez et al, 2001a;Perry et al, 2005a;Silva et al, 2011Silva et al, , 2017. As pulmonary NECs were already found in lungfish (Zaccone et al, 1989(Zaccone et al, , 1997Kemp et al, 2003), it is possible that the exposure to aerial hypoxia stimulated air-breathing in these animals via external O 2 chemoreceptors in the lungs rather than internal O 2 chemoreceptorshowever, at least in the case of P. aethiopicus, such air-breathing response is eliminated by complete gill denervation (Lahiri et al, 1970).…”