To boldly gulp: standard metabolic rate and boldness have context-dependent influences on risk-taking to breathe air in a catfish

Abstract

The African sharptooth catfish Clarias gariepinus has bimodal respiration, it has a suprabranchial air-breathing organ alongside substantial gills. We used automated bimodal respirometry to reveal that undisturbed juvenile catfish (N=29) breathed air continuously in normoxia, with a marked diurnal cycle. Air breathing and routine metabolic rate (RMR) increased in darkness when, in the wild, this nocturnal predator forages. Aquatic hypoxia (20% air saturation) greatly increased overall reliance on air breathing. We investigated whether two measures of risk taking to breathe air, namely absolute rates of aerial O 2 uptake (Ṁ O2,air ) and the percentage of RMR obtained from air (%Ṁ O2,air ), were influenced by individual standard metabolic rate (SMR) and boldness. In particular, whether any influence varied with resource availability (normoxia versus hypoxia) or relative fear of predation (day versus night). Individual SMR, derived from respirometry, had an overall positive influence on Ṁ O2,air across all contexts but a positive influence on %Ṁ O2,air only in hypoxia. Thus, a pervasive effect of SMR on air breathing became most acute in hypoxia, when individuals with higher O 2 demand took proportionally more risks. Boldness was estimated as time required to resume air breathing after a fearful stimulus in daylight normoxia (T res ). Although T res had no overall influence on Ṁ O2,air or %Ṁ O2,air , there was a negative relationship between T res and %Ṁ O2,air in daylight, in normoxia and hypoxia. There were two T res response groups, 'bold' phenotypes with T res below 75 min (N=13) which, in daylight, breathed proportionally more air than 'shy' phenotypes with T res above 115 min (N=16). Therefore, individual boldness influenced air breathing when fear of predation was high. Thus, individual energy demand and personality did not have parallel influences on the emergent tendency to take risks to obtain a resource; their influences varied in strength with context.

Heritability of Boldness and Hypoxia Avoidance in European Seabass, Dicentrarchus labrax

“…Indeed, the hypoxia avoidance test encompasses the willingness to take risk and individual hypoxia sensibility hereby linking with an additional component through the respiratory metabolism. These results evidence complex links between boldness and hypoxia tolerance as demonstrated by Killen et al, [73] and McKenzie et al, [75], confirming that some behaviors are context specific [9]. Further, this absence of cross context consistency may be explained by the fact that correlations between behavioral responses in different contexts are generated by selection pressures partially alleviated in rearing environment and in domesticated species when compared to the wild environment [76].…”

Evolutionary and cardio‐respiratory physiology of air‐breathing and amphibious fishes

“…The African sharptooth catfish, Clarias gariepinus, has been the focus of some studies to investigate associations among metabolic rate, risk-taking to breathe air, and behavioural tendencies. 102,103 Despite the limited number of studies, the results reveal interesting patterns that will, hopefully, stimulate further research in this field. C. gariepinus breathes air using a suprabranchial structure termed the arborescent organ.…”

“…103 Individual standard metabolic rate in C. gariepinus was strongly correlated with rates of oxygen uptake from the air, especially when surfacing might be perceived as inherently risky (daylight) and also when water oxygen levels drop (aquatic hypoxia). 103 Thus, metabolic rate may be a driver of overall rates of risk-taking, although this seems self-evident since we know that air-breathing responses are driven by chemoreflexes. 86 Chemoreceptors may assure the link to metabolic rate in areas of the venous vasculature where blood oxygen levels reflect rates of oxygen removal by respiring tissues and stimulate surfacing reflexes more frequently in animals with high tissue oxygen demand.…”

“…86 Chemoreceptors may assure the link to metabolic rate in areas of the venous vasculature where blood oxygen levels reflect rates of oxygen removal by respiring tissues and stimulate surfacing reflexes more frequently in animals with high tissue oxygen demand. 83,89,90,103 However, individual standard metabolic rate was also positively correlated with boldness measured in two contexts, namely the time-lag to resume air-breathing after a startle stimulus in their respirometer (T-res) and the time-lag to enter the centre of a novel environment measured in an open field test. 103 These latter two measures of boldness were very highly correlated between themselves.…”

Life in a bubble: the role of the labyrinth organ in determining territory, mating and aggressive behaviours in anabantoids

“…Air-breathing fishes are on a spectrum, spanning from facultative to obligate air-breathers. Facultative air breathers do not typically breathe air and mostly only do so when dissolved oxygen (DO) is low or when oxygen demands are high, but see McKenzie et al (2015) for exceptions. In contrast, obligate air breathers use aerial respiration at all times, regardless of aquatic conditions or their oxygen demands, due to their reduced gill surface areas.…”