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

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

The interplay between aerobic metabolism and antipredator performance: vigilance is related to recovery rate after exercise

When attacked by a predator, fish respond with a sudden fast-start motion away from the threat. Although this anaerobically-powered swimming necessitates a recovery phase which is fueled aerobically, little is known about links between escape performance and aerobic traits such as aerobic scope (AS) or recovery time after exhaustive exercise. Slower recovery ability or a reduced AS could make some individuals less likely to engage in a fast-start response or display reduced performance. Conversely, increased vigilance in some individuals could permit faster responses to an attack but also increase energy demand and prolong recovery after anaerobic exercise. We examined how AS and the ability to recover from anaerobic exercise relates to differences in fast-start escape performance in juvenile golden gray mullet at different acclimation temperatures. Individuals were acclimated to either 18, 22, or 26°C, then measured for standard and maximal metabolic rates and AS using intermittent flow respirometry. Anaerobic capacity and the time taken to recover after exercise were also assessed. Each fish was also filmed during a simulated attack to determine response latency, maximum speed and acceleration, and turning rate displayed during the escape response. Across temperatures, individuals with shorter response latencies during a simulated attack are those with the longest recovery time after exhaustive anaerobic exercise. Because a short response latency implies high preparedness to escape, these results highlight the trade-off between the increased vigilance and metabolic demand, which leads to longer recovery times in fast reactors. These results improve our understanding of the intrinsic physiological traits that generate inter-individual variability in escape ability, and emphasize that a full appreciation of trade-offs associated with predator avoidance and energy balance must include energetic costs associated with vigilance and recovery from anaerobic exercise

The role of physiological traits in assortment among and within fish shoals

Individuals of gregarious species often group with conspecifics to which they are phenotypically similar. This among-group assortment has been studied for body size, sex and relatedness. However, the role of physiological traits has been largely overlooked. Here, we discuss mechanisms by which physiological traits—particularly those related to metabolism and locomotor performance—may result in phenotypic assortment not only among but also within animal groups. At the among-group level, varying combinations of passive assortment, active assortment, phenotypic plasticity and selective mortality may generate phenotypic differences among groups. Even within groups, however, individual variation in energy requirements, aerobic and anaerobic capacity, neurological lateralization and tolerance to environmental stressors are likely to produce differences in the spatial location of individuals or associations between group-mates with specific physiological phenotypes. Owing to the greater availability of empirical research, we focus on groups of fishes (i.e. shoals and schools). Increased knowledge of physiological mechanisms influencing among- and within-group assortment will enhance our understanding of fundamental concepts regarding optimal group size, predator avoidance, group cohesion, information transfer, life-history strategies and the evolutionary effects of group membership. In a broader perspective, predicting animal responses to environmental change will be impossible without a comprehensive understanding of the physiological basis of the formation and functioning of animal social groups. This article is part of the themed issue ‘Physiological determinants of social behaviour in animals’

Male sexually coercive behaviour drives increased swimming efficiency in female guppies

Sexual coercion of females by males is widespread across sexually reproducing species. It stems from a conflict of interest over reproduction and exerts selective pressure on both sexes. For females, there is often a significant energetic cost of exposure to male sexually coercive behaviours. Our understanding of the efficiency of female resistance to male sexually coercive behaviour is key to understanding how sexual conflict contributes to population level dynamics and ultimately to the evolution of sexually antagonistic traits. Overlooked within this context are plastic physiological responses of traits within the lifetime of females that could moderate the energetic cost imposed by coercive males. Here, we examined whether conflict over the frequency and timing of mating between male and female guppies Poecilia reticulata can induce changes in swimming performance and aerobic capacity in females as they work to escape harassment by males. Females exposed to higher levels of harassment over a 5-month period used less oxygen to swim at a given speed, but displayed no difference in resting metabolic rate, maximal metabolic rate, maximal sustained swimming speed or aerobic scope compared to females receiving lower levels of harassment. The observed increase in swimming efficiency is at least partially related to differences in swimming mechanics, likely brought on by a training effect of increased activity, as highly harassed females spent less time performing pectoral fin-assisted swimming. Sexual conflict results in sexually antagonistic traits that impose a variety of costs, but our results show that females can reduce costs through phenotypic plasticity. It is also possible that phenotypic plasticity in swimming physiology or mechanics in response to sexual coercion can potentially give females more control over matings and affect which male traits are under selection

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

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 O2 uptake (ṀO2,air) and the percentage of RMR obtained from air (%ṀO2,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 ṀO2,air across all contexts but a positive influence on %ṀO2,air only in hypoxia. Thus, a pervasive effect of SMR on air breathing became most acute in hypoxia, when individuals with higher O2 demand took proportionally more risks. Boldness was estimated as time required to resume air breathing after a fearful stimulus in daylight normoxia (Tres). Although Tres had no overall influence on ṀO2,air or %ṀO2,air, there was a negative relationship between Tres and %ṀO2,air in daylight, in normoxia and hypoxia. There were two Tres response groups, ‘bold’ phenotypes with Tres below 75 min (N=13) which, in daylight, breathed proportionally more air than ‘shy’ phenotypes with Tres 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

Overview of a Disease Outbreak and Introduction of a Step-by-Step Protocol for the Eradication of Mycobacterium haemophilum in a Zebrafish System

In 2017, the zebrafish unit at University of Glasgow experienced a detrimental outbreak of pathogenic bacterium, Mycobacterium haemophilum. The presence of other bacterial species was also confirmed by bacteriology growth in the same unit. The affected individuals composed of a wild-origin parental population sourced from India and their F1 offspring generation. Bacteria were diagnostically confirmed to be present systemically in fish and within the water and biofilm of the recirculating zebrafish system. In the absence of a publicly accessible step-by-step disinfectant protocol for these difficult-to-eliminate pathogens, we devised a successful procedure to eradicate mycobacteria and Aeromonas species after colony removal using Cleanline Chlorine tablets (active ingredient Sodium dichloroisocyanurate) and Virkon Aquatic®. Postdisinfection diagnostics did not detect pathogens in the system or in the new fish inhabiting the system that were tested. Newly established fish colonies have not shown similar clinical signs or disease-induced mortality in the 1-year period following system disinfection and repopulation. We present a historical background of the bacterial outbreak and a disinfection method which can be replicated in other zebrafish facilities—at small or large scales—for reliable mycobacterium removal. This procedure can be implemented as a disinfection protocol before the introduction of a new fish population to a previously contaminated system

The relationship between metabolic rate and sociability is altered by food-deprivation

Individuals vary in the extent to which they associate with conspecifics, but little is known about the energetic underpinnings of this variation in sociability. Group-living allows individuals to find food more consistently, but within groups, there can be competition for food items. Individuals with an increased metabolic rate could display decreased sociability to reduce competition. Long-term food deprivation (FD) may alter any links between sociability and metabolic rate by affecting motivation to find food. We examined these issues in juvenile qingbo carp Spinibarbus sinensis, to understand how FD and metabolic rate affect sociability. Like many aquatic ectotherms, this species experiences seasonal bouts of FD. Individuals were either: (i) food-deprived for 21 days; or (ii) fed a maintenance ration (control). Fish from each treatment were measured for standard metabolic rate (SMR) and tested for sociability twice: once in the presence of a control stimulus shoal and once with a food-deprived stimulus shoal. Control individuals ventured further from stimulus shoals over a 30-min trial, while food-deprived fish did not change their distance from stimulus shoals as trials progressed. Control fish with a higher SMR were least sociable. Well-fed controls showed decreased sociability when exposed to food-deprived stimulus shoals, but there was evidence of consistency in relative sociability between exposures to different shoal types. Results contrast with previous findings that several days of fasting causes individuals to decrease associations with conspecifics. Prolonged FD may cause individuals to highly prioritize food acquisition, and the decreased vigilance that would accompany continuous foraging may heighten the need for the antipredator benefits of shoaling. Conversely, decreased sociability in well-fed fish with a high SMR probably minimizes intraspecific competition, allowing them to satisfy an increased energetic demand while foraging. Together, these results suggest that FD – a challenge common for many ectothermic species – can affect individual sociability as well as the attractiveness of groups towards conspecifics. In addition, the lack of a link between SMR and sociability in food-deprived fish suggests that, in situations where group membership is linked to fitness, the extent of correlated selection on metabolic traits may be context-dependent

Fish swimming in schools save energy regardless of their spatial position

For animals, being a member of a group provides various advantages, such as reduced vulnerability to predators, increased foraging opportunities and reduced energetic costs of locomotion. In moving groups such as fish schools, there are benefits of group membership for trailing individuals, who can reduce the cost of movement by exploiting the flow patterns generated by the individuals swimming ahead of them. However, whether positions relative to the closest neighbours (e.g. ahead, sided by side or behind) modulate the individual energetic cost of swimming is still unknown. Here, we addressed these questions in grey mullet Liza aurata by measuring tail-beat frequency and amplitude of 15 focal fish, swimming in separate schools, while swimming in isolation and in various positions relative to their closest neighbours, at three speeds. Our results demonstrate that, in a fish school, individuals in any position have reduced costs of swimming, compared to when they swim at the same speed but alone. Although fish swimming behind their neighbours save the most energy, even fish swimming ahead of their nearest neighbour were able to gain a net energetic benefit over swimming in isolation, including those swimming at the front of a school. Interestingly, this energetic saving was greatest at the lowest swimming speed measured in our study. Because any member of a school gains an energetic benefit compared to swimming alone, we suggest that the benefits of membership in moving groups may be more strongly linked to reducing the costs of locomotion than previously appreciated

The Role of Individual Heterogeneity in Collective Animal Behaviour

Social grouping is omnipresent in the animal kingdom. Considerable research has focused on understanding how animal groups form and function, including how collective behaviour emerges via self-organising mechanisms and how phenotypic variation drives the behaviour and functioning of animal groups. However, we still lack a mechanistic understanding of the role of phenotypic variation in collective animal behaviour. Here we present a common framework to quantify individual heterogeneity and synthesise the literature to systematically explain and predict its role in collective behaviour across species, contexts, and traits. We show that individual heterogeneity provides a key intermediary mechanism with broad consequences for sociality (e.g., group structure, functioning), ecology (e.g., response to environmental change), and evolution. We also outline a roadmap for future research

Metabolic costs of feeding predictively alter the spatial distribution of individuals in fish schools

Group living is ubiquitous among animals [1, 2], but the exact benefits of group living experienced by individual groupmates is related to their spatial location within the overall group [3, 4, 5]. Individual variation in behavioral traits and nutritional state is known to affect interactions between individuals and their social group [6, 7], but physiological mechanisms underpinning collective animal behavior remain largely unexplored [8]. Here, we show that while fish at the front of moving groups are most successful at capturing food items, these individuals then show a systematic, post-feeding movement toward the rear of groups. Using observations of fish feeding in groups coupled with estimates of metabolic rate in fish consuming different meal sizes, we demonstrate that the magnitude of this shift in spatial position is directly related to the aerobic metabolic scope remaining after accounting for energetic costs of digestion. While previous work has shown that hungry individuals occupy anterior positions in moving groups [9, 10], our results show that the metabolic demand of food processing reduces the aerobic capacity available for locomotion in individuals that eat most, thus preventing them from maintaining leading positions. This basic trade-off between feeding and locomotor capacity could fundamentally dictate the spatial position of individuals within groups, perhaps obviating the role of individual traits in determining spatial preferences over shorter timescales (e.g., hours to days). This may be a general constraint for individuals within animal collectives, representing a key, yet overlooked, mediator of group functioning that could affect leadership, social information transfer, and group decision making