Thinking Fish

The current issue of Behavioural Processes is specially themed around the subject of fish cognition. Articles cover “swarm intelligence,” personality, and memory in fish, as well as their numerical abilities and behavioral plasticity across social contexts. Taken in concert, this research highlights how this huge taxa (comprising more than half of all vertebrate species, dispersed across a stunning range of aquatic environments) provides a basis for theorizing sociality. The explicit focus is on thinking, with the shared goal of “uncovering the mechanisms by which these cognitive feats are achieved, tracing the evolution of different behavioural solutions to environmental challenges, and charting the conditions under which various abilities are displayed.” But given the welter of issues around cognition and sociality—how they seem to ratchet each other up—and the challenge fish intelligence presents to assumptions about brain size and complex thought, these evolutionary concerns hardly exhaust the potential relevance of these findings.

The broader register for intelligence is subjectivity, and for fish, this register now seems quite substantive. They can divide attention when foraging and have long-term and episodic-like memories; they with develop time-place associations and form complex spatial representations of their environments, including learning its geometry. As well, some species form and use tools in flexible ways; they demonstrate audience effects in modulating their foraging and may engage in elaborate courtship displays. All of this indicates an interpretive and performative subject. What are the social dimensions of this subjectivity?

The answer depends, in part, on how this new research stands up against other taxon that have been privileged for analyzing sociality, but also in our abilities to overcome human bias against recognizing fish as sentient. Ethologist Jonathan Balcombe argues that these prejudices turn on perceptions of primitiveness in fish—though, in evolutionary terms, “about half of fish species are no more ‘primitive’ than we are” (2016:21). But he also rails against “our cerebrocentric view of intelligence,” which disparages their relatively small brains; even though, their ratio of brain weight to body weight is advantageous in the buoyant medium of water, which “frees aquatic organisms from the ravages of weight on terrestrial creatures” (12). These entwined conceits and misperceptions may well be challenged now, the editors of this issue opine, as “the recorded abilities of fish have been quickly catching up to those of better-studied taxa.” To the extent that they are emerging as model organisms for understanding complex, emergent phenomenon like swarming behavior.

The basis for this modeling potential is that fish are socially developed: the taxa features grouping habits in many species, from breeding pairs to schools of tens of thousands. Such groups often feature collective movement and decision-making (with hunting, especially), and formation of complex social networks and or hierarchies. Fundamental in all of this is the capacity for individual recognition; as Balcombe summarizes, “they recognize other individuals by sight, smell, voice, and other sensory channels; they choose mates nonrandomly; and they cooperate.” Such modalities of individuality are a complex function of the elaboration of sociality, and this is becoming evident in fish. The editors observe, “it is likely that in group-living species the personality composition of a group also has a large effect on the success of its members,” and that increasing “variance in behavior among individuals may be advantageous for groups, resulting in selective forces that maintain variation in personality.” The editors are mostly concerned with elucidating mechanisms driving all this at the genetic, neuronal, and behavioral levels. But the links between behavioral ecology and cognition in fish don’t stop there. The immense adaptive variation across the taxa suggests diversity of social articulations as well, in which these behavioral forms emerge and are reproduced. Fish may well become valorized model organisms for how all this plays out, not just in aquariums but in watery “fields,” as well.

Abstracts

Noam Miller, “Cognition in Fishes,” Behavioural Processes 141, no. 2 (August 2017): 137-140, https://doi.org/10.1016/j.beproc.2017.03.013.

Christos C. Ioannou, “Swarm Intelligence in Fish? The Difficulty in Demonstrating Distributed and Self-organised Collective Intelligence in (Some) Animal Groups,” Behavioural Processes 141, no. 2 (August 2017): 141-151, https://doi.org/10.1016/j.beproc.2016.10.005.

Larger groups often have a greater ability to solve cognitive tasks compared to smaller ones or lone individuals. This is well established in social insects, navigating flocks of birds, and in groups of prey collectively vigilant for predators. Research in social insects has convincingly shown that improved cognitive performance can arise from self-organised local interactions between individuals that integrates their contributions, often referred to as swarm intelligence. This emergent collective intelligence has gained in popularity and been directly applied to groups of other animals, including fish. Despite being a likely mechanism at least partially explaining group performance in vertebrates, I argue here that other possible explanations are rarely ruled out in empirical studies. Hence, evidence for self-organised collective (or ‘swarm’) intelligence in fish is not as strong as it would first appear. These other explanations, the ‘pool-of-competence’ and the greater cognitive ability of individuals when in larger groups, are also reviewed. Also discussed is why improved group performance in general may be less often observed in animals such as shoaling fish compared to social insects. This review intends to highlight the difficulties in exploring collective intelligence in animal groups, ideally leading to further empirical work to illuminate these issues.

Sigal Balshine, Marian Y. L. Wong, and Adam R. Reddon, “Social Motivation and Conflict Resolution Tactics as Potential Building Blocks of Sociality in Cichlid Fishes,” Behavioural Processes 141, no. 2 (August 2017): 152-160, https://doi.org/10.1016/j.beproc.2017.01.001.

Even closely related and ecologically similar cichlid species of Lake Tanganyika exhibit an impressive diversity of social systems, and therefore these fishes offer an excellent opportunity to examine the evolution of social behaviour. Sophisticated social relationships are thought to have evolved via a building block design where more fundamental social behaviours and cognitive processes have been combined, incrementally modified, and elaborated over time. Here, we studied two of these putative social building blocks in two closely related species of cichlids: Neolamprologus pulcher, a group-living species, and Telmatochromis temporalis, a non-grouping species. Otherwise well matched in ecology, this pair of species provide an excellent comparison point to understand how behavioural processes may have been modified in relation to the evolution of sociality. Using social assays in both the laboratory and in the field, we explored each species’ motivation to interact with conspecifics, and each species’ conflict resolution tactics. We found that individuals of the group living species, N. pulcher, displayed higher social motivation and were more likely to produce submission displays than were individuals of the non-grouping species, T. temporalis. We argue that the motivation to interact with conspecifics is a necessary prerequisite for the emergence of group living, and that the use of submission reduces the costs of conflict and facilitates the maintenance of close social proximity. These results suggest that social motivation and conflict resolution tactics are associated with social complexity, and that these behavioural traits may be functionally significant in the evolution and maintenance of sociality.

Christian Agrillo, Maria Elena Miletto Petrazzini, and Angelo Bisazza, “Numerical Abilities in Fish: A Methodological Review,” Behavioural Processes 141, no. 2 (August 2017): 161-171, https://doi.org/10.1016/j.beproc.2017.02.001.

The ability to utilize numerical information can be adaptive in a number of ecological contexts including foraging, mating, parental care, and anti-predator strategies. Numerical abilities of mammals and birds have been studied both in natural conditions and in controlled laboratory conditions using a variety of approaches. During the last decade this ability was also investigated in some fish species. Here we reviewed the main methods used to study this group, highlighting the strengths and weaknesses of each of the methods used. Fish have only been studied under laboratory conditions and among the methods used with other species, only two have been systematically used in fish—spontaneous choice tests and discrimination learning procedures. In the former case, the choice between two options is observed in a biologically relevant situation and the degree of preference for the larger/smaller group is taken as a measure of the capacity to discriminate the two quantities (e.g., two shoals differing in number). In discrimination learning tasks, fish are trained to select the larger or the smaller of two sets of abstract objects, typically two-dimensional geometric figures, using food or social companions as reward. Beyond methodological differences, what emerges from the literature is a substantial similarity of the numerical abilities of fish with those of other vertebrates studied.

Caroline M. DeLong, Stephanie Barbato, Taylor O’Leary, and K. Tyler Wilcox, “Small and Large Number Discrimination in Goldfish (Carassius auratus) with Extensive Training,” Behavioural Processes 141, no. 2 (August 2017): 172-183, https://doi.org/10.1016/j.beproc.2016.11.011.

Previous studies on relative quantity discrimination in birds and mammals with training procedures have employed hundreds or thousands of trials whereas studies with fish typically use dozens of trials. The goal of this study was to examine whether more extensive training improves the performance of fish tested on stimuli in the small (< 4) and large (> 4) number range. Goldfish were trained with dot array stimuli using the ratio 0.5 (2 vs. 4, 6 vs. 12) across two blocks of training sessions with a total of approximately 1200 trials. They were tested after each block of training sessions with the ratios 0.33 (1 vs. 3, 5 vs. 15), 0.5 (2 vs. 4, 6 vs. 12), and 0.67 (2 vs. 3, 10 vs. 15). Performance exceeded 90% correct on both test blocks. Accuracy was not affected by manipulating the surface area, density, or space of stimuli. Performance was best on the ratio 0.5 in test block 1, but ratio-independent in test block 2. There was no difference in performance in the small vs. large number range across the study. These results suggest that fish given extensive training can achieve accuracy on a numerical task comparable to well-trained birds, humans, or non-human primates.

Tyrone Lucon-Xiccato and Angelo Bisazza, “Individual Differences in Cognition among Teleost Fishes,” Behavioural Processes 141, no. 2 (August 2017): 184-195, https://doi.org/10.1016/j.beproc.2017.01.015.

Individual differences in cognitive abilities have been thoroughly investigated in humans and to a lesser extent in other mammals. Despite the growing interest in studying cognition in other taxonomic groups, data on individual differences are scarce for non-mammalian species. Here, we review the literature on individual differences in cognitive abilities in teleost fishes. Relatively few studies have directly addressed this topic and have provided evidence of consistent and heritable individual variation in cognitive abilities in fish. We found much more evidence of individual cognitive differences in other research areas, namely sex differences, personality differences, cerebral lateralisation and comparison between populations. Altogether, these studies suggest that individual differences in cognition are as common in fish as in warm–blooded vertebrates. Based on the example of research on mammals, we suggest directions for future investigation in fish.

Olivia L. Guayasamin, Iain D. Couzin, and Noam Y. Miller, “Behavioural Plasticity across Social Contexts is Regulated by the Directionality of Inter-individual Differences,” Behavioural Processes 141, no. 2 (August 2017): 196-204, https://doi.org/10.1016/j.beproc.2016.10.004.

An individual’s behavioural phenotype is a combination of its unique behavioural propensities and its responsiveness to environmental variation, also known as behavioural plasticity. In social species, we must not only explore how individuals respond to variations in the physical environment but also how they react to changes in their social environment. A growing body of work has demonstrated that the behavioural heterogeneity of a group can alter its responsiveness, decision making, and fitness. Whether an individual is more or less extreme than a partner—what we term its ‘relative personality’—may also alter individual behavioural responses. We determined exploratory tendencies of individual zebrafish (Danio rerio) and then constructed pairs with varying differences in ‘relative personality’ to determine the effect of differences between partners on behavioural plasticity. We find that relative personality, but not the magnitude of the difference between partners, is the most important determinant of behavioural plasticity across social treatments. Despite this overall effect, pairs of fish exhibited no predictable leader-follower interactions, suggesting that details of the experimental paradigm may be important in shaping social dynamics.

I. Barber, A. B. Mora, E. M. Payne, K. L. Weinersmith, and A. Sih, “Parasitism, Personality and Cognition in Fish,” Behavioural Processes 141, no. 2 (August 2017): 205-219, https://doi.org/10.1016/j.beproc.2016.11.012.

It is well established that parasites can have profound effects on the behaviour of host organisms, and that individual differences in behaviour can influence susceptibility to parasite infections. Recently, two major themes of research have developed. First, there has been a growing interest in the proximate, mechanistic processes underpinning parasite-associated behaviour change, and the interactive roles of the neuro-, immune, and other physiological systems in determining relationships between behaviour and infection susceptibility. Secondly, as the study of behaviour has shifted away from one-off measurements of single behaviours and towards a behavioural syndromes/personality framework, research is starting to focus on the consequences of parasite infection for temporal and contextual consistency of behaviour, and on the implications of different personality types for infection susceptibility. In addition, there is increasing interest in the potential for relationships between cognition and personality to also have implications for host-parasite interactions. As models well-suited to both the laboratory study of behaviour and experimental parasitology, teleost fish have been used as hosts in many of these studies. In this review we provide a broad overview of the range of mechanisms that potentially generate links between fish behaviour, personality, and parasitism, and illustrate these using examples drawn from the recent literature. In addition, we examine the potential interactions between cognition, personality and parasitism, and identify questions that may be usefully investigated with fish models.

S. L. White, T. Wagner, C. Gowan, and V. A. Braithwaite, “Can Personality Predict Individual Differences in Brook Trout Spatial Learning Ability?,” Behavioural Processes 141, no. 2 (August 2017): 220-228, https://doi.org/10.1016/j.beproc.2016.08.009.

While differences in individual personality are common in animal populations, understanding the ecological significance of variation has not yet been resolved. Evidence suggests that personality may influence learning and memory; a finding that could improve our understanding of the evolutionary processes that produce and maintain intraspecific behavioural heterogeneity. Here, we tested whether boldness, the most studied personality trait in fish, could predict learning ability in brook trout. After quantifying boldness, fish were trained to find a hidden food patch in a maze environment. Stable landmark cues were provided to indicate the location of food and, at the conclusion of training, cues were rearranged to test for learning. There was a negative relationship between boldness and learning as shy fish were increasingly more successful at navigating the maze and locating food during training trials compared to bold fish. In the altered testing environment, only shy fish continued using cues to search for food. Overall, the learning rate of bold fish was found to be lower than that of shy fish for several metrics suggesting that personality could have widespread effects on behaviour. Because learning can increase plasticity to environmental change, these results have significant implications for fish conservation.

Darya A. Meshalkina, Marina N. Kizlyk, Elana V. Kysil, Adam D. Collier, David J. Echevarria, Murilo S. Abreu, Leonardo J. G. Barcellos, Cai Song, and Allan V. Kalueff, “Understanding Zebrafish Cognition,” Behavioural Processes 141, no. 2 (August 2017): 229-241, https://doi.org/10.1016/j.beproc.2016.11.020.

Zebrafish (Danio rerio) are rapidly becoming a popular model organism in translational and cognitive neuroscience research. Both larval and adult zebrafish continue to increase our understanding of cognitive mechanisms and their genetic and pharmacological modulation. Here, we discuss the developing utility of zebrafish in understanding cognitive phenotypes and their deficits, relevant to a wide range human brain disorders. We also discuss the potential of zebrafish models for high-throughput genetic mutant and small molecule screening (e.g., amnestics, cognitive enhancers, neurodevelopmental/neurodegenerative drugs), which becomes critical for identifying novel candidate genes and molecular drug targets to treat cognitive deficits. In addition to discussing the existing challenges and future strategic directions in this field, we emphasize how zebrafish models of cognitive phenotypes continue to form an interesting and rapidly emerging new field in neuroscience.

Robert Gerlai, “Zebrafish and Relational Memory: Could a Simple Fish Be Useful for the Analysis of Biological Mechanisms of Complex Vertebrate Learning?,” Behavioural Processes 141, no. 2 (August 2017): 242-250, https://doi.org/10.1016/j.beproc.2017.01.016.

Analysis of the zebrafish allows one to combine two distinct scientific approaches, comparative ethology and neurobehavioral genetics. Furthermore, this species arguably represents an optimal compromise between system complexity and practical simplicity. This mini-review focuses on a complex form of learning, relational learning and memory, in zebrafish. It argues that zebrafish are capable of this type of learning, and it attempts to show how this species may be useful in the analysis of the mechanisms and the evolution of this complex brain function. The review is not intended to be comprehensive. It is a short opinion piece that reflects the author’s own biases, and it draws some of its examples from the work coming from his own laboratory. Nevertheless, it is written in the hope that it will persuade those who have not utilized zebrafish and who may be interested in opening their research horizon to this relatively novel but powerful vertebrate research tool.

David J. White, Eliza Watts, Kelsey Pitchforth, Samuel Agyapong, and Noam Miller, “‘Sociability’ Affects the Intensity of Mate-Choice Copying in Female Guppies, Poecilia reticulata,” Behavioural Processes 141, no. 2 (August 2017): 251-257, https://doi.org/10.1016/j.beproc.2017.02.017.

Selecting a quality mate can involve acquiring and accessing large amounts of information; information that can be obtained either independently or socially. One means of learning about mates socially is to attend to other members of one's sex and copy their mate choices. It is possible however that not all individuals of a species benefit equally from, or are equally effective at, copying. We examined whether female guppies copied the mate choices of other females. Then, in a separate context we measured each female's ‘sociability’: their proclivity to affiliate with other guppies. In the mate-choice copying procedure, ‘focal’ females chose to spend time near two putative mates. Next, focals observed another (model) female interact with the focal's non-preferred male. Finally, the focal again chose between the same two males. For sociability, we examined the time focal females spent near a trio of other guppies. Females did indeed mate copy: they spent more time with their non-preferred male when a model female had been seen interacting with that male. The effect however was highly variable. Sociability significantly predicted the intensity of mate-choice copying. Results suggest that individuals vary consistently in the types of information they use when making mating decisions.