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Physiology

Oxygen favours the bold

McKenzie, D.J., Belão, T.C., Killen, S.S., and Rantin, F.T. (2015). To boldly gulp: standard metabolic rate and boldness have context-dependent influences on risk-taking to breathe air in a catfish. J. Exp. Biol. 218: 3762-3770. doi: 10.1242/jeb.122903

Air-breathing in fishes

Most aquatic organisms rely on only gills to exchange oxygen and carbon dioxide between their bodies and the surrounding water. A minority of fishes (<2% of known species) also have accessory respiratory structures, allowing them to exchange gases directly with air (Fig. 1). These structures are quite diverse: some fish use what is known as a labyrinth (a heavily-vascularized, folded bone located above the gills), some have a primitive lung, and a few use their skin to breathe air.

The few fishes capable of bimodal respiration (air- and water-breathing) are often native to challenging environments with low or unpredictable water oxygen levels. Since air has far more oxygen than a comparable volume of water, accessory organs provide a reliable secondary source of an indispensable resource. Some of these fish, termed obligate air-breathers, have come to rely so heavily on air that, like mammals and birds, will drown without consistent access to the surface.

Fig.1. Some air-breathing fishes. Top: an African sharptooth catfish, the species featured in the JEB paper (Clarias gariepinus, left), and a northern snakehead (Channa argus, right). Bottom: the Florida gar (Lepisosteus platyrhincus, left) and a common betta fish (Betta splendens, right). Photo credits: Wikimedia, S. Tam (quest4fish), and F. Geiser (Flickr).

Fig.1. Some air-breathing fishes. Top: an African sharptooth catfish, the species featured in the JEB paper (Clarias gariepinus, left), and a northern snakehead (Channa argus, right). Bottom: the Florida gar (Lepisosteus platyrhincus, left) and a common betta fish (Betta splendens, right). Photo credits: Wikimedia, S. Tam (quest4fish), and F. Geiser (Flickr).

While many air-breathers are found in hazardous swamps and distant jungles, they are not all quite so exotic. The pet store staples, bettas (the Siamese fighting fish, Betta splendens), are labyrinth fish and regularly gulp atmospheric air. It’s one of the reasons why these beautiful animals can be in housed in such tiny aquaria.

Life’s a gamble

A successful gulp means avoiding aerial predators. Image: Pixabay

A successful air gulp means avoiding aerial predators, especially birds. Image: Pixabay

Coming to the surface to gulp air can be dangerous: bottom-dwellers must leave the safety of their hiding places, putting themselves at greater risk from predators of the land, sea, or air. Accordingly, the paper by McKenzie et al. demonstrates that even the boldest catfish are not thrill-seekers, and adjust their frequency of gulping based upon context. Factoring into this decision is (1) how much the individual catfish actually needs to breathe air, (2) how risky it is to breathe air, and (3) how much risk the individual catfish will accept to breathe air. 

McKenzie et al. explored the complex interplay between physiology, environmental factors , and individual personality by tracking air-breathing over the daily light cycle in both oxygen-rich (normoxic) and oxygen-poor water (hypoxia). Individual variation in air-breathing was matched with fish energy demands (resting oxygen consumption rate) and boldness to get a sense of how each of these factors influenced catfish behaviour.

Individual energy demands

High resting oxygen consumption rates indicate greater energetic demands. Since most cellular energy is converted into its usable form (ATP) in an oxygen-dependent process (aerobic metabolism), and ATP levels are carefully maintained in healthy cells, animals that use a lot of energy have to consume more oxygen for their cells to match ATP supply with demands (Fig. 2). Catfish with high energy demands tend to gulp more, since air-breathing is more effective method of gas exchange than gill ventilation. Similarly, there is a clear daily rhythm, such that air-breathing is more common at night, when these nocturnal hunters actively forage for food and burn more energy.

A successful gulp means avoiding aerial predators. Image: Pixabay

A successful gulp means avoiding aerial predators. Image: Pixabay

Environmental influences

In addition to its physiology, an individual’s situation also influences how often it gulps air. When water oxygen content is poor (aquatic hypoxia), catfish rely more heavily upon their alternative oxygen source. Additionally, when catfish perceive the environment is more dangerous (in daylight, when they are more likely to be seen by predators), they tend to avoid air-breathing.

Fig. 3. Proportion of oxygen consumption (% of MO2) attributable to air-breathing across contexts in representative bold and timid personality types. Catfish tend to air-breathe more at night due to both increased activity and possibly reduced predation pressure. Hypoxia (low water oxygen content) reduces the resting oxygen consumption rate of catfish, but induces a greater reliance on the alternative method of oxygen uptake. Bold and timid animals respond similarly to environmental cues, though the former tends to show more exaggerated responses, since they have both a greater resting oxygen consumption and extract a greater proportion of their total oxygen requirements from air. Image for Oceanbites by B.G. Borowiec, based upon data presented by McKenzie et al., 2015.

Fig. 3. Proportion of oxygen consumption (% of MO2) attributable to air-breathing across contexts in representative bold and timid personality types. Catfish tend to air-breathe more at night due to both increased activity and possibly reduced predation pressure. Hypoxia (low water oxygen content) reduces the resting oxygen consumption rate of catfish, but induces a greater reliance on the alternative method of oxygen uptake. Bold and timid animals respond similarly to environmental cues, though the former tends to show more exaggerated responses, since they have both a greater resting oxygen consumption and extract a greater proportion of their total oxygen requirements from air. Image for Oceanbites by B.G. Borowiec, based upon data presented by McKenzie et al., 2015.

Personality

Personality determines how an individual interprets cues in its environment and interacts with the world, including deciding when to air-breathe. In this study, bold or timid personalities were assigned based upon how long it took the individual fish to resume air-breathing after being startled in a daylight environment. Bold animals recovered from the scare and resumed air-breathing much more quickly (<75 mins) than timid animals (>115 mins).

Bold animals tend to have higher metabolic rates than explained by their body size alone, indicating greater routine oxygen needs. Though the exact causal relationship between temperament and energetic demands is unclear, bold animals are generally thought to be more active and aggressive across a number of species. It’s no surprise then that bold fish extract a greater proportion of their oxygen needs from air-breathing, and that this was consistent across light levels and dissolved oxygen content (Fig. 3).

Personality in the ocean

Should I stay or should I go? Image: Pixabay.

Should I stay or should I go? Image: Pixabay.

Air-breathing is a rare thing in fishes, and is best studied in a few well-known, freshwater examples like Amazonian catfish, lungfish, and the bowfin. Context-dependent decision-making, however, is a much broader concept. The decision of a clownfish to peek out from the anemone refugee, or an eel’s ambush of a crab scurrying just a little too close to its burrow, likely follows similar principles as a catfish emerging from the river bottom to breathe air. The potential benefits of an action are weighed against its consequences, and these can be modified both by the specific situation and the animal’s physiology.

Brittney G. Borowiec
Brittney is a PhD candidate at McMaster University in Hamilton, ON, Canada, and joined Oceanbites in September 2015. Her research focuses on the physiological mechanisms and evolution of the respiratory and metabolic responses of Fundulus killifish to intermittent (diurnal) patterns of hypoxia.

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