Yes,correct context is indeed the key: An answer to Haave‐Audet et al. 2019

We published a study recently testing the link between brain size and behavioural plasticity using brain size selected guppy (Poecilia reticulata) lines (2019, Journal of Evolutionary Biology, 32, 218‐226). Only large‐brained fish showed habituation to a new, but actually harmless environment perceived as risky, by increasing movement activity over the 20‐day observation period. We concluded that “Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level”. In a commentary published in the same journal, Haave‐Audet et al. challenged the main message of our study, stating that (a) relative brain size is not a suitable proxy for cognitive ability and (b) habituation measured by us is likely not adaptive and costly. In our response, we first show that a decade's work has proven repeatedly that relative brain size is indeed positively linked to cognitive performance in our model system. Second, we discuss how switching from stressed to unstressed behaviour in stressful situations without real risk is likely adaptive. Finally, we point out that the main cost of behavioural plasticity in our case is the development and maintenance of the neural system needed for information processing, and not the expression of plasticity. We hope that our discussion with Haave‐Audet et al. helps clarifying some central issues in this emerging research field.     

The integration of sociality,monoamines and stress neuroendocrinology in fish models: applications in the neurosciences

Animal‐focused research has been crucial for scientific advancement, but rodents are still taking a starring role. Starting as merely supporting evidence found in rodents, the use of fish models has slowly taken a more central role and expanded its overall contributions in areas such as social sciences, evolution, physiology and recently in translational medical research. In the neurosciences, zebrafish Danio rerio have been widely adopted, contributing to our understanding of the genetic control of brain processes and the effects of pharmacological manipulations. However, discussion continues regarding the paradox of function versus structure, when fishes and mammals are compared and on the potentially evolutionarily conserved nature of behaviour across fish species. From a behavioural standpoint, we explore aversive–stress and social behaviour in selected fish models and refer to the extensive contributions of stress and monoaminergic systems. We suggest that, in spite of marked neuroanatomical differences between fishes and mammals, stress and sociality are conserved at the behavioural and molecular levels. We also suggest that stress and sociality are mediated by monoamines in predictable and non‐trivial ways and that monoamines could bridge the relationship between stress and social behaviour. To reconcile the level of divergence with the level of similarity, we need neuroanatomical, pharmacological, behavioural and ecological studies conducted in the laboratory and in nature. These areas need to add to each other to enhance our understanding of fish behaviour and ultimately how this all may lead to better model systems for translational studies.     

Social plasticity in fish: integrating mechanisms and function

Social plasticity is a ubiquitous feature of animal behaviour. Animals must adjust the expression of their social behaviour to the nuances of daily social life and to the transitions between life‐history stages, and the ability to do so affects their Darwinian fitness. Here, an integrative framework is proposed for understanding the proximate mechanisms and ultimate consequences of social plasticity. According to this framework, social plasticity is achieved by rewiring or by biochemically switching nodes of the neural network underlying social behaviour in response to perceived social information. Therefore, at the molecular level, it depends on the social regulation of gene expression, so that different brain genomic and epigenetic states correspond to different behavioural responses and the switches between states are orchestrated by signalling pathways that interface the social environment and the genotype. At the evolutionary scale, social plasticity can be seen as an adaptive trait that can be under positive selection when changes in the environment outpace the rate of genetic evolutionary change. In cases when social plasticity is too costly or incomplete, behavioural consistency can emerge by directional selection that recruits gene modules corresponding to favoured behavioural states in that environment. As a result of this integrative approach, how knowledge of the proximate mechanisms underlying social plasticity is crucial to understanding its costs, limits and evolutionary consequences is shown, thereby highlighting the fact that proximate mechanisms contribute to the dynamics of selection. The role of teleosts as a premier model to study social plasticity is also highlighted, given the diversity and plasticity that this group exhibits in terms of social behaviour. Finally, the proposed integrative framework to social plasticity also illustrates how reciprocal causation analysis of biological phenomena (i.e. considering the interaction between proximate factors and evolutionary explanations) can be a more useful approach than the traditional proximate–ultimate dichotomy, according to which evolutionary processes can be understood without knowledge on proximate causes, thereby black‐boxing developmental and physiological mechanisms.     

Habitat-dependent and -independent plastic responses to social environment in the nine-spined stickleback (Pungitius pungitius) brain

The influence of environmental complexity on brain development has been demonstrated in a number of taxa, but the potential influence of social environment on neural architecture remains largely unexplored. We investigated experimentally the influence of social environment on the development of different brain parts in geographically and genetically isolated and ecologically divergent populations of nine-spined sticklebacks (Pungitius pungitius). Fish from two marine and two pond populations were reared in the laboratory from eggs to adulthood either individually or in groups. Group-reared pond fish developed relatively smaller brains than those reared individually, but no such difference was found in marine fish. Group-reared fish from both pond and marine populations developed larger tecta optica and smaller bulbi olfactorii than individually reared fish. The fact that the social environment effect on brain size differed between marine and pond origin fish is in agreement with the previous research, showing that pond fish pay a high developmental cost from grouping while marine fish do not. Our results demonstrate that social environment has strong effects on the development of the stickleback brain, and on the brain''s sensory neural centres in particular. The potential adaptive significance of the observed brain-size plasticity is discussed.     

Environmental enrichment promotes neural plasticity and cognitive ability in fish

Different kinds of experience during early life can play a significant role in the development of an animal''s behavioural phenotype. In natural contexts, this influences behaviours from anti-predator responses to navigation abilities. By contrast, for animals reared in captive environments, the homogeneous nature of their experience tends to reduce behavioural flexibility. Studies with cage-reared rodents indicate that captivity often compromises neural development and neural plasticity. Such neural and behavioural deficits can be problematic if captive-bred animals are being reared with the intention of releasing them as part of a conservation strategy. Over the last decade, there has been growing interest in the use of environmental enrichment to promote behavioural flexibility in animals that are bred for release. Here, we describe the positive effects of environmental enrichment on neural plasticity and cognition in juvenile Atlantic salmon (Salmo salar). Exposing fish to enriched conditions upregulated the forebrain expression of NeuroD1 mRNA and improved learning ability assessed in a spatial task. The addition of enrichment to the captive environment thus promotes neural and behavioural changes that are likely to promote behavioural flexibility and improve post-release survival.     

Walter Heiligenberg: the jamming avoidance response and beyond

Walter Heiligenberg (1938–1994) was an exceptionally gifted behavioral physiologist who made enormous contributions to the analysis of behavior and to our understanding of how the brain initiates and controls species-typical behavioral patterns. He was distinguished by his rigorous analytical approach used in both behavioral studies and neuroethological investigations. Among his most significant contributions to neuroethology are a detailed analysis of the computational rules governing the jamming avoidance response in weakly electric fish and the elucidation of the principal neural pathway involved in neural control of this behavior. Based on his work, the jamming avoidance response is perhaps the best-understood vertebrate behavior pattern in terms of the underlying neural substrate. In addition to this pioneering work, Heiligenberg stimulated research in a significant number of other areas of ethology and neuroethology, including: the quantitative assessment of aggressivity in cichlid fish; the ethological analysis of the stimulus–response relationship in the chirping behavior of crickets; the exploration of the neural and endocrine basis of communicatory behavior in weakly electric fish; the study of cellular mechanisms of neuronal plasticity in the adult fish brain; and the phylogenetic analysis of electric fishes using a combination of morphology, electrophysiology, and mitochondrial sequence data.T. H. Bullock: deceased 2005     

Effect of the early social environment on behavioural and genomic responses to a social challenge in a cooperatively breeding vertebrate

The early social environment can have substantial, lifelong effects on vertebrate social behaviour, which can be mediated by developmental plasticity of brain gene expression. Early‐life effects can influence immediate behavioural responses towards later‐life social challenges and can activate different gene expression responses. However, while genomic responses to social challenges have been reported frequently, how developmental experience influences the shape of these genomic reaction norms remains largely unexplored. We tested how manipulating the early social environment of juvenile cooperatively breeding cichlids, Neolamprologus pulcher, affects their behavioural and brain genomic responses when competing over a resource. Juveniles were reared either with or without a breeder pair and a helper. Fish reared with family members behaved more appropriately in the competition than when reared without. We investigated whether the different social rearing environments also affected the genomic responses to the social challenge. A set of candidate genes, coding for hormones and receptors influencing social behaviour, were measured in the telencephalon and hypothalamus. Social environment and social challenge both influenced gene expression of egr‐1 (early growth response 1) and gr1 (glucocorticoid receptor 1) in the telencephalon and of bdnf (brain‐derived neurotrophic factor) in the hypothalamus. A global analysis of the 11 expression patterns in the two brain areas showed that neurogenomic states diverged more strongly between intruder fish and control fish when they had been reared in a natural social setting. Our results show that same molecular pathways may be used differently in response to a social challenge depending on early‐life experiences.     

Aggression Level in Different Water Velocities Depends on Population Origin in Grayling, Thymallus thymallus

Phenotypic plasticity is recognized as an important mechanism of adaptation. However, because of its potential costs and limits, it has been hypothesized to be reduced and ultimately become lost when there is no selection for its maintenance. Heterogeneous environments in particular are expected to favour and thus maintain plastic phenotypes. Lakes and rivers differ in their flow regimes. In addition to higher average water velocity, rivers are characterized by distinct spatial and temporal variation in water flow, whereas lakes can be regarded as quite uniform in this respect. We studied whether behaviour, which is generally considered to be highly plastic, shows differences in the degree of plasticity between lake and river populations of the European grayling, Thymallus thymallus, fry in response to different water velocities. Given that aggressive behaviour in fish has been shown to relate to ambient flow regime, we compared aggressiveness of hatchery‐reared grayling originating from hatchery stocks of two lake and two river populations in still and flowing water. River fish showed higher aggressiveness in flowing water compared with still water, whereas aggressiveness of lake fish did not appear to vary according to water velocity. The higher plasticity of aggressiveness evoked in river fish by different water velocities may thus represent an adaptation to more variable flow and presumably related feeding conditions in their natural environment.     

The role of learning in fish behaviour

Summary The behavioural patterns of fish are the result of innate (built-in) patterns of maturation (developmental changes) and of learning processes (imprinting and trial-and-error learning). Innate behavioural patterns are considered to be hard-wired and inflexible. However, through learning, fish can adapt to environmental change. For instance, the homing behaviour of fish may be partly the result of the development of specific parts of the brain and partly because of changes in behaviour with experience. Similarly, one can assume that the feeding mode of fish involving snap-responses is innate, but learning enables fish to modify their foraging behaviour in response to a fluctuating environment. By reviewing these and other examples, such as the role of recognition learning and socially transmitted behaviour, one can illustrate the importance of learning in the everyday life of fishes. Although learning plays a large role in the behaviour of fishes, the learning capacity of fishes may also be useful to fisheries research and hatchery operations.     

Simultaneous biologging of heart rate and acceleration, and their relationships with energy expenditure in free-swimming sockeye salmon (Oncorhynchus nerka)

Monitoring the physiological status and behaviour of free-swimming fishes remains a challenging task, although great promise stems from techniques such as biologging and biotelemetry. Here, implanted data loggers were used to simultaneously measure heart rate (f _H), visceral temperature, and a derivation of acceleration in two groups of wild adult sockeye salmon (Oncorhynchus nerka) held at two different water speeds (slow and fast). Calibration experiments performed with individual fish in a swim tunnel respirometer generated strong relationships between acceleration, f _H, tail beat frequency and energy expenditure over a wide range of swimming velocities. The regression equations were then used to estimate the overall energy expenditure of the groups of fish held at different water speeds. As expected, fish held at faster water speeds exhibited greater f _H and acceleration, and correspondingly a higher estimated energy expenditure than fish held at slower water speeds. These estimates were consistent with gross somatic energy density of fish at death, as determined using proximate analyses of a dorsal tissue sample. Heart rate alone and in combination with acceleration, rather than acceleration alone, provided the most accurate proxies for energy expenditure in these studies. Even so, acceleration provided useful information on the behaviour of fish and may itself prove to be a valuable proxy for energy expenditure under different environmental conditions, using a different derivation of the acceleration data, and/or with further calibration experiments. These results strengthen the possibility that biologging or biotelemetry of f _H and acceleration may be usefully applied to migrating sockeye salmon to monitor physiology and behaviour, and to estimate energy use in the natural environment.     

Life stage dependent responses to desiccation risk in the annual killifish Nothobranchius wattersi

To assess whether the annual killifish Nothobranchius wattersi responds plastically to a desiccation risk and whether this response is life stage dependent, life‐history traits such as maturation time, fecundity and life span were experimentally measured in N. wattersi that were subjected to a drop in water level either as juveniles, as adults or both as juveniles and adults. Fish that were exposed to simulated pool drying as juveniles did not show changes in reproductive output or life span. Adults reacted by doubling short term egg deposition at the cost of a shorter lifespan. Overall, these results suggest that annual fish species can use phenotypic plasticity to maximize their reproductive output when faced with early pond drying, but this response appears to be life‐stage specific. In addition to frogs and aquatic insects, phenotypic plasticity induced by forthcoming drought is now also confirmed in annual fishes and could well be a common feature of the limited number of fish taxa that manage to survive in this extreme environment.     

Coping strategies in a strongly schooling fish,the common carp Cyprinus carpio

Individual common carp Cyprinus carpio were screened repeatedly for risk taking (rate of exploration of a novel, potentially dangerous environment) and for competitive ability (success in gaining access to a spatially restricted food source). Marked differences in behaviour were evident, and significant consistency in individual responses across trials was found for both risk taking and competitive ability. In addition, there was a significant positive relationship between individual performance in these two contexts, with fish that explored more quickly in the novel environment tending to be among the first to gain access to restricted food. In two follow‐up studies, resting metabolic rate, blood lactate and glucose and the expression of the cortisol receptor gene in the head kidney and brain were compared in fish from the two extremes of the risk‐taking spectrum. Mass‐specific metabolic rate was significantly higher in risk‐taking than in risk‐avoiding fish, while plasma lactate and glucose concentrations and expression of the cortisol receptor gene were lower. It was concluded that a behavioural syndrome based on boldness and aggression exists in C. carpio, as it does in many other animals, and that this is associated with differences in metabolic and stress physiology (down to the genomic level) similar to those described in animals with different coping strategies.     

Brain‐encysting trematodes and altered monoamine activity in naturally infected killifish Fundulus parvipinnis

This paper presents novel evidence to address mechanisms by which trematode parasites effect behavioural changes in naturally infected fish hosts. California killifish Fundulus parvipinnis infected with the brain‐encysting trematode Euhaplorchis californiensis display conspicuous swimming behaviours that render them 30 times more likely to be eaten by birds, the parasite's final host. Prevalence of E. californiensis reaches nearly 100% in most F. parvipinnis populations, with parasite biomass constituting almost 2% of F. parvipinnis biomass in some locations. Despite having thousands of cysts on their brains, infected fish grow and mature at rates comparable to those of uninfected populations. The lack of general pathology combined with the specificity of the altered behaviours suggests that the behavioural changes are due to parasite manipulation. The monoamine neurotransmitters serotonin and dopamine, which control locomotion and social behaviour in fishes and other vertebrates, were examined to explore the underlying mechanisms of this behaviour modification. Whereas previous studies were similarly conducted with experimentally infected fish, in this study, brain dopaminergic and serotonergic activity were analysed in naturally infected fish to assess how E. californiensis may alter F. parvipinnis monoamines in a naturally occurring system. A parasite density‐associated decrease in serotonergic activity occurred in the hippocampus of naturally infected fish, as well as a decrease in dopaminergic activity in the raphe nuclei, suggesting that E. californiensis inhibits serotonin and dopamine signaling in naturally infected F. parvipinnis. The neurochemical profile of infected fish is consistent with the hypothesis that E. californiensis affects brain monoaminergic systems in order to induce impulse‐driven, active, and aggressive behaviour in its hosts.     

Ecosystem consequences of fish parasites*

In most aquatic ecosystems, fishes are hosts to parasites and, sometimes, these parasites can affect fish biology. Some of the most dramatic cases occur when fishes are intermediate hosts for larval parasites. For example, fishes in southern California estuaries are host to many parasites. The most common of these parasites, Euhaplorchis californiensis, infects the brain of the killifish Fundulus parvipinnis and alters its behaviour, making the fish 10–30 times more susceptible to predation by the birds that serve as its definitive host. Parasites like E. californiensis are embedded in food webs because they require trophic transmission. In the Carpinteria Salt Marsh estuarine food web, parasites dominate the links and comprise substantial amount of biomass. Adding parasites to food webs alters important network statistics such as connectance and nestedness. Furthermore, some free‐living stages of parasites are food items for free‐living species. For instance, fishes feed on trematode cercariae. Being embedded in food webs makes parasites sensitive to changes in the environment. In particular, fishing and environmental disturbance, by reducing fish populations, may reduce parasite populations. Indirect evidence suggests a decrease in parasites in commercially fished species over the past three decades. In addition, environmental degradation can affect fish parasites. For these reasons, parasites in fishes may serve as indicators of environmental impacts.     

Context is key: A comment on Herczeg et al. 2019

In the last several years, there has been a surge in the number of studies addressing the causes and consequences of among‐individual variation in cognitive ability and behavioural plasticity. Here, we use a recent publication by Herczeg et al. (2019: 32(3), 218–226) to highlight three shortcomings common to this newly emerging field. In their study, Herczeg et al. attempted to link variation in cognitive ability and behavioural plasticity by testing whether selection lines of guppies (Poecilia reticulata) that differ in relative brain size also differ in behavioural plasticity, as might be expected if the costs to plasticity are predominantly derived from the cost of developing large brains. First, residual brain size may not be a suitable proxy for ‘cognitive ability’. Recent work has shown that intraspecific variation in cognitive ability can be better understood by considering variation in the specific brain areas responsible for the relevant behaviours as opposed to whole‐brain mass. Second, the measure of behavioural plasticity, habituation, is unlikely to fulfil the assumptions that plasticity is both adaptive and costly. Finally, we point out several misconceptions regarding animal personality that continue to contribute to the choice of traits that are not well aligned with study objectives. Elucidating the mechanisms underlying among‐individual variation in cognition and behavioural plasticity within populations requires integration between behavioural ecology and comparative cognition, and the study system developed by Herczeg et al. has the potential to provide important mechanistic insights. We hope that by articulating and critically appraising the underlying assumptions that are common in these traditionally separate disciplines, a strong foundation can emerge to allow for more fruitful integration of these fields.     

Brain size predicts behavioural plasticity in guppies (Poecilia reticulata): An experiment

Understanding how animal personality (consistent between‐individual behavioural differences) arises has become a central topic in behavioural sciences. This endeavour is complicated by the fact that not only the mean behaviour of individuals (behavioural type) but also the strength of their reaction to environmental change (behavioural plasticity) varies consistently. Personality and cognitive abilities are linked, and we suggest that behavioural plasticity could also be explained by differences in brain size (a proxy for cognitive abilities), since accurate decisions are likely essential to make behavioural plasticity beneficial. We test this idea in guppies (Poecilia reticulata), artificially selected for large and small brain size, which show clear cognitive differences between selection lines. To test whether those lines differed in behavioural plasticity, we reared them in groups in structurally enriched environments and then placed adults individually into empty tanks, where we presented them daily with visual predator cues and monitored their behaviour for 20 days with video‐aided motion tracking. We found that individuals differed consistently in activity and risk‐taking, as well as in behavioural plasticity. In activity, only the large‐brained lines demonstrated habituation (increased activity) to the new environment, whereas in risk‐taking, we found sensitization (decreased risk‐taking) in both brain size lines. We conclude that brain size, potentially via increasing cognitive abilities, may increase behavioural plasticity, which in turn can improve habituation to novel environments. However, the effects seem to be behaviour‐specific. Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level.     

Identifying reproductive events using archival tags: egg‐laying behaviour of the small spotted catshark Scyliorhinus canicula

The use of archival depth telemetry as a means of remotely assessing the reproductive rates of free‐ranging fishes is explored. This is achieved by electronically tracking the vertical movements of individual female small spotted catsharks Scyliorhinus canicula in the natural environment, whilst simultaneously evaluating the temporal and vertical distributions of egg‐laying in this species. Distinctive patterns of short‐term (0·3–3·7 h), shallow‐water activity are documented in the time–depth profiles of female S. canicula that occur at an appropriate depth (1·0–2·3 m) and periodicity (every 10–12 days) to represent egg‐laying behaviour. Putative egg‐laying behaviour was exhibited simultaneously by two individually tracked female S. canicula during late‐spring and early‐summer. The results highlight that, provided species behaviour is suitable and complementary methods such as previous data, laboratory experiments and field surveys can be used to validate the patterns observed, archival depth telemetry offers an unobtrusive means by which egg production and egg‐laying behaviour of free‐living fishes can be estimated. As precise information regarding life‐history parameters is difficult to obtain for free‐ranging fish species, this technique could be used to improve the parameterization of species demographic models that are relevant to the management of wild fish populations.