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.
Phenotypic variation is selectively maintained in populations and pervades animal social systems.Considerable evidence shows that phenotypic differences among grouping animals drive the behaviour, structure, and functioning of animal groups.This individual heterogeneity may thus be a key intermediary mechanism that regulates collective behaviour.We lack a unified understanding to explain and predict the role of individual heterogeneity across different species, contexts, and traits.An objective quantification of individual heterogeneity in physiological, cognitive, and behavioural components provides a common framework for understanding individual heterogeneity and its social, ecological, and evolutionary consequences.
The current effects of global warming on marine ecosystems are predicted to increase, with species responding by changing their spatial distributions. Marine ectotherms such as fish experience ...elevated distribution shifts, as temperature plays a key role in physiological functions and delineating population ranges through thermal constraints. Distributional response predictions necessary for population management have been complicated by high heterogeneity in magnitude and direction of movements, which may be explained by both biological as well as methodological study differences. To date, however, there has been no comprehensive synthesis of the interacting ecological factors influencing fish distributions in response to climate change and the confounding methodological factors that can affect their estimation. In this study we analyzed published studies meeting criteria of reporting range shift responses to global warming in 115 taxa spanning all major oceanic regions, totaling 595 three‐dimensional population responses (latitudinal, longitudinal, and depth), with temperature identified as a significant driver. We found that latitudinal shifts were the fastest in non‐exploited, tropical populations, and inversely correlated with depth shifts which, in turn, dominated at the trailing edges of population ranges. While poleward responses increased with rate of temperature change and latitude, niche was a key factor in predicting both depth (18% of variation) and latitudinal responses (13%), with methodological predictors explaining between 10% and 28% of the observed variance in marine fish responses to temperature change. Finally, we found strong geographical publication bias and limited taxonomical scope, highlighting the need for more representative and standardized research in order to address heterogeneity in distribution responses and improve predictions in face of changing climate.
In this study we analyzed published articles reporting range shift responses to global warming in marine fish, totaling 595 depth and latitudinal responses. We identified differences in distribution shifts due to ecological variables such as niche affinity, rate of sea temperature change, and commercial exploitation, as well as methodological biases due to different approaches in estimating and reporting range shifts.
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’.
Most animals experience temperature variations as they move through the environment. For ectotherms, in particular, temperature has a strong influence on habitat choice. While well studied at the ...species level, less is known about factors affecting the preferred temperature of individuals; especially lacking is information on how physiological traits are linked to thermal preference and whether such relationships are affected by factors such feeding history and growth trajectory. This study examined these issues in the common minnow Phoxinus phoxinus, to determine the extent to which feeding history, standard metabolic rate (SMR) and aerobic scope (AS), interact to affect temperature preference. Individuals were either: 1) food deprived (FD) for 21 days, then fed ad libitum for the next 74 days; or 2) fed ad libitum throughout the entire period. All animals were then allowed to select preferred temperatures using a shuttle‐box, and then measured for SMR and AS at 10 °C, estimated by rates of oxygen uptake. Activity within the shuttle‐box under a constant temperature regime was also measured. In both FD and control fish, SMR was negatively correlated with preferred temperature. The SMR of the FD fish was increased compared with the controls, probably due to the effects of compensatory growth, and so these growth‐compensated fish preferred temperatures that were on average 2·85 °C cooler than controls fed a maintenance ration throughout the study. Fish experiencing compensatory growth also displayed a large reduction in activity. In growth‐compensated fish and controls, activity measured at 10 °C was positively correlated with preferred temperature. Individual fish prefer temperatures that vary predictably with SMR and activity level, which are both plastic in response to feeding history and growth trajectories. Cooler temperatures probably allow individuals to reduce maintenance costs and divert more energy towards growth. A reduction in SMR at cooler temperatures, coupled with a decrease in spontaneous activity, could also allow individuals to increase surplus AS for coping with environmental stressors. In warming climates, however, aquatic ectotherms could experience frequent fluctuations in food supply with long‐lasting effects on metabolic rate due to compensatory growth, while simultaneously having limited access to preferred cooler habitats.
Ecology Letters (2010) 13: 184-193 Metabolic energy fuels all biological processes, and therefore theories that explain the scaling of metabolic rate with body mass potentially have great predictive ...power in ecology. A new model, that could improve this predictive power, postulates that the metabolic scaling exponent (b) varies between 2/3 and 1, and is inversely related to the elevation of the intraspecific scaling relationship (metabolic level, L), which in turn varies systematically among species in response to various ecological factors. We test these predictions by examining the effects of lifestyle, swimming mode and temperature on intraspecific scaling of resting metabolic rate among 89 species of teleost fish. As predicted, b decreased as L increased with temperature, and with shifts in lifestyle from bathyal and benthic to benthopelagic to pelagic. This effect of lifestyle on b may be related to varying amounts of energetically expensive tissues associated with different capacities for swimming during predator-prey interactions.
•Stressors amplify physiological and behavioural links by increasing variation.•Stressors can attenuate such relationships by decreasing variation.•These mechanisms stem from differing sensitivity to ...stressors among phenotypes.•These influences underlie a range of ecological phenomena.•They could also be important for evolutionary responses to environmental change.
Although correlations have frequently been observed between specific physiological and behavioural traits across a range of animal taxa, the nature of these associations has been shown to vary. Here we argue that a major source of this inconsistency is the influence of environmental stressors, which seem capable of revealing, masking, or modulating covariation in physiological and behavioural traits. These effects appear to be mediated by changes in the observed variation of traits and differential sensitivity to stressors among phenotypes. Considering that wild animals routinely face a range of biotic and abiotic stressors, increased knowledge of these effects is imperative for understanding the causal mechanisms of a range of ecological phenomena and evolutionary responses to stressors associated with environmental change.
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.
ABSTRACT Evidence of behavioural sleep has been observed in every animal species studied to date, but current knowledge of the behaviour, neurophysiology and ecophysiology associated with sleep is ...concentrated on mammals and birds. Fish are a hugely diverse group that can offer novel insights into a variety of sleep-related behaviours across environments, but the ecophysiological relevance of sleep in fish has been largely overlooked. Here, we systematically reviewed the literature to assess the current breadth of knowledge on fish sleep, and surveyed the diverse physiological effects and behaviours associated with sleep. We also discuss possible ways in which unstudied external factors may alter sleep behaviours. For example, predation risk may alter sleep patterns, as has been shown in mammalian, avian and reptilian species. Other environmental factors – such as water temperature and oxygen availability – have the potential to alter sleep patterns in fish differently than for terrestrial endotherms. Understanding the ecological influences on sleep in fish is vital, as sleep deprivation has the potential to affect waking behaviour and fitness owing to cognitive and physiological impairments, possibly affecting ecological phenomena and sensitivity to environmental stressors in ways that have not been considered.
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 3–5. ...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.
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•We examined individual positioning in groups of swimming fish after feeding•Fish that ate most subsequently shifted to more posterior positions within groups•Shifts in position were related to the remaining aerobic scope after feeding•Feeding-related constraints could affect leadership and group functioning
The mechanisms of how individuals spatially arrange themselves within social groups remain unclear. Using observations of fish feeding in groups and estimates of metabolic rate, McLean et al. show that shifts in position within groups after feeding are related to aerobic metabolic scope remaining after accounting for energetic costs of digestion.
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