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

Silva, Glauber S. F. da; Ventura, Daniela A.D.N.; Zena, Lucas A.; Giusti, Humberto; Glass, Mogens L.; Klein, Wilfried

doi:10.1016/j.cbpa.2017.03.001

Cited by 7 publications

(5 citation statements)

References 49 publications

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“…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.…”

Section: Discussionmentioning

confidence: 99%

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

Pineda

Aragao

McKenzie

et al. 2020

Journal of Experimental Biology

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In some fishes, the ability to breathe air has evolved to overcome constraints in hypoxic environments but comes at a cost of increased predation. To reduce this risk, some species perform group air breathing. Temperature may also affect the frequency of air breathing in fishes, but this topic has received relatively little research attention. This study examined how acclimation temperature and acute exposure to hypoxia affected the air-breathing behaviour of a social catfish, the bronze corydoras Corydoras aeneus, to determine whether individual oxygen demand influenced the behaviour of entire groups. Groups of seven fish were observed in an arena to measure air-breathing frequency of individuals and consequent group air-breathing behaviour, under three oxygen concentrations (100%, 60%, 20% air saturation) and two acclimation temperatures (25°C & 30°C). Intermittent flow respirometry was used to estimate oxygen demand of individuals. Increasingly severe hypoxia increased air-breathing at the individual and group levels. While there were minimal differences in air-breathing frequency among individuals in response to an increase in temperature, the effect of temperature that did exist manifested as an increase in group air-breathing frequency at 30°C. Groups that were more socially cohesive during routine activity took more breaths but, in most cases, air-breathing among individuals this was not temporally clustered. There was no association between an individual's oxygen demand and its air-breathing frequency in a group. For Corydoras aeneus, while air-breathing frequency is influenced by hypoxia, behavioural variation among groups could explain the small overall effect of temperature on group air-breathing frequency.

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Section: Discussionmentioning

confidence: 99%

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

Pineda

Aragao

McKenzie

et al. 2020

Journal of Experimental Biology

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“…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).…”

Section: Systemic Factorsmentioning

confidence: 99%

“…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.…”

Section: Environmental Factorsmentioning

confidence: 99%

“…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 .…”

Section: Environmental Factorsmentioning

confidence: 99%

“…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).…”

Section: O 2 Chemoreceptorsmentioning

confidence: 99%

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

et al. 2018

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This review considers the environmental and systemic factors that can stimulate air-breathing responses in fishes with bimodal respiration, and how these may be controlled by peripheral and central chemoreceptors. The systemic factors that stimulate air-breathing in fishes are usually related to conditions that increase the O demand of these animals (e.g. physical exercise, digestion and increased temperature), while the environmental factors are usually related to conditions that impair their capacity to meet this demand (e.g. aquatic/aerial hypoxia, aquatic/aerial hypercarbia, reduced aquatic hidrogenionic potential and environmental pollution). It is now well-established that peripheral chemoreceptors, innervated by cranial nerves, drive increased air-breathing in response to environmental hypoxia and/or hypercarbia. These receptors are, in general, sensitive to O and/or CO/H levels in the blood and/or the environment. Increased air-breathing in response to elevated O demand may also be driven by the peripheral chemoreceptors that monitor O levels in the blood. Very little is known about central chemoreception in air-breathing fishes, the data suggest that central chemosensitivity to CO/H is more prominent in sarcopterygians than in actinopterygians. A great deal remains to be understood about control of air-breathing in fishes, in particular to what extent control systems may show commonalities (or not) among species or groups that have evolved air-breathing independently, and how information from the multiple peripheral (and possibly central) chemoreceptors is integrated to control the balance of aerial and aquatic respiration in these animals.

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Control of Breathing in Ectothermic Vertebrates

Milsom

Gilmour

Perry

et al. 2022

Comprehensive Physiology

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The ectothermic vertebrates are a diverse group that includes the Fishes (Agnatha, Chondrichthyes, and Osteichthyes), and the stem Tetrapods (Amphibians and Reptiles). From an evolutionary perspective, it is within this group that we see the origin of air-breathing and the transition from the use of water to air as a respiratory medium. This is accompanied by a switch from gills to lungs as the major respiratory organ and from oxygen to carbon dioxide as the primary respiratory stimulant. This transition first required the evolution of bimodal breathing (gas exchange with both water and air), the differential regulation of O 2 and CO 2 at multiple sites, periodic or intermittent ventilation, and unsteady states with wide oscillations in arterial blood gases. It also required changes in respiratory pump muscles (from buccopharyngeal muscles innervated by cranial nerves to axial muscles innervated by spinal nerves). The question of the extent to which common mechanisms of respiratory control accompany this progression is an intriguing one. While the ventilatory control systems seen in all extant vertebrates have been derived from common ancestors, the trends seen in respiratory control in the living members of each vertebrate class reflect both shared-derived features (ancestral traits) as well as unique specializations. In this overview article, we provide a comprehensive survey of the diversity that is seen in the afferent inputs (chemo and mechanoreceptor), the central respiratory rhythm generators, and the efferent outputs (drive to the respiratory pumps and valves) in this group.

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

Cited by 7 publications

References 49 publications

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

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

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

Control of Breathing in Ectothermic Vertebrates

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