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Contemporary Topics in Fish Cognition and Behaviour

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Contemporary Topics in Fish Cognition and Behaviour Available online at www.sciencedirect.com ScienceDirect Contemporary topics in fish cognition and behaviour Catarina Vila Pouca and Culum Brown The field of fish cognition and behaviour is now well established with numerosity), understand the accuracy and upper and recent developments reflect a shift to mechanistic, limit of their discrimination ability, and assess how fish comparative and theoretical approaches compared to early compare to other vertebrate species (reviewed in Ref. work. In this review we briefly summarise recent advances in [6]). The general consensus from this work is that fish four major areas of research: spatial learning, social cognition, have good number sense and can be as efficient in numerical competency and cognition, consciousness and pain. establishing quantity as terrestrial vertebrates. The debate on whether fish are conscious and able to feel pain is particularly topical, and we discuss recent behavioural and Two numerical information processing systems seem to adaptive arguments in favour of fish pain. In this review we also exist in humans: a generalist ‘analogue magnitude sys- propose interesting avenues of research in which fish have tem’ to estimate large quantities; and an accurate ‘object been given little attention in comparison with other vertebrate tracking system’, to quickly track small quantities indi- species. vidually. Recent studies have sought to understand if these also occur in fish (reviewed in Ref. [6]). In line with Address other non-human animals, some studies on fish support Department of Biological Sciences, Macquarie University, Sydney 2109, the dual system hypothesis (e.g. [7]), and the unit limit of Australia the ‘object tracking system’ of fishes seems to be similar to other vertebrates (around four objects, set by short- Corresponding author: Brown, Culum ([email protected]) term memory). Nonetheless, a few studies provide sup- port for an alternative perspective, that a single processing Current Opinion in Behavioral Sciences 2017, 16:46–52 system could operate across all quantities (e.g. [8,9]), thus This review comes from a themed issue on Mixed emotions leaving the subject unresolved and open to further study. Edited by Ben Hayden and Jessica F Cantlon Fish are capable of true numerical discrimination like other species, but will spontaneously use continuous quantities if available [10,11]. Their accuracy and upper http://dx.doi.org/10.1016/j.cobeha.2017.03.002 discrimination limit is comparable to those of mammals 2352-1546/ã 2017 Elsevier Ltd. All rights reserved. and birds, with some species-specific differences [6,12–15]. Three-spined sticklebacks, for example, were successful in a discrimination task where they choose the larger of two social groups with a ratio of 0.86 (i.e. there is small relative difference between quantities), similar to bottlenose dolphins [8,16]. It also appears that, when Introduction learning to distinguish between quantities, fish sponta- Fish have now become a standard model species in the neously learn about relative sizes (this is bigger than that) study of comparative cognition (Figure 1). Comprehen- instead of absolute sizes (this has four elements and that sive reviews on fish behaviour and cognition, with has two), even though they are capable of both [17], and detailed methodologies used in this research, are avail- can even learn using ordinal numerical information able and we refer readers new to this field to those reviews (choose the nth element; [18]). [1,2 ,3 ,4]. The objective of this short review is to summarise developments in four major areas of contem- Researchers have also begun investigating proximate porary research in fish cognition, as well as highlight some mechanisms of numerical discrimination such as the role exciting new directions in less studied topics (Box 1). of individual, sex, cerebral lateralization and context differences [9,13,19,20]. For example, guppies that were Numerical discrimination strongly lateralized had better numerical skills than non- Numbers are an essential part of everyday life for most lateralized fish, both in the context of shoal size choice animals. Being able to count or assess quantities can guide and training with abstract stimuli [20], and their numeri- decisions such as which group to join, where to forage or cal acuity was enhanced when two guppies were inter- whether to fight or flee (see Ref. [5]). This is also true for acting, as a result of meritocratic leadership [21]. fish, and indeed they show good numerical skills. The main focus of research in numerical competency in fish Another emerging theme in human and non-human has been to distinguish quantity discrimination from literature is whether numerical discrimination is indepen- numerical abilities (by controlling other cues that covary dent of sensory modalities. Evidence in other species is Current Opinion in Behavioral Sciences 2017, 16:46–52 www.sciencedirect.com Evolving topics in fish cognition and behaviour Vila Pouca and Brown 47 Figure 1 50 40 30 20 10 Number of publications 0 1993 1994 2003 2004 2010 2011 2012 2013 2014 2015 2016 Year Current Opinion in Behavioral Sciences The number of publications on fish learning and cognition grew in recent decades and currently seems to be reaching stability. Data based on keyword search (fish, fishes, learn, learning and cognition) in Google Scholar. The 2016?data excludes publications from November and December. still inconclusive [22], and in fish only one study has modality-dependent systems for numerical skills in fishes addressed this issue. Blind cavefish could distinguish but far more work needs to be done in this area [14]. It is between groups of sticks up to a ratio of 0.50 (two versus also a possibility that specific selective pressures acted on six and two versus four sticks), but were unsuccessful blind cavefish to decrease metabolic consumption, when tested with a 0.67 ratio (two versus three sticks), a reducing brain mass or dropping neural circuits related ratio achieved by other fish species using vision [14]. to cognitive tasks not useful in caves, such as shoal size These results are compatible with the idea of multiple discrimination [14]. One good approach to tackle ultimate and proximate questions for numerical discrimination would be to use species that are active in both good Box 1 New lines of research in fish cognition. and poor light conditions, such as weakly electric fish, and Cognitive flexibility is one emergent area of research. While only a test them with visual and other sensory cues [14]. few species have been studied, it seems fish are capable of inhibiting previously learned behaviours, of reversal learning (e.g. [58]), and display innovative behaviours and problem solving in new situations Social cognition (e.g. [59]). Fish would be a good model species to test evolutionary Complex social intelligence is no longer considered ecology predictions such as the ‘necessity drives innovation’ hypothesis, and investigate potential mechanisms underlying beha- restricted to primates. Complex social behaviours in fish vioural flexibility [60,61]. have been widely acknowledged and reviewed and Another topic largely unexplored is the study of play behaviour in include social learning and traditions, individual recogni- fish. For long deemed restricted to primates, it has become clear tion, cooperation and shared intentionality, dominance other species of mammals and birds also play. Playful behaviour hierarchies, social status and transitive inference, among seems to be a developmental precursor to many behavioural and many others [1,4]. social skills, and might facilitate innovation and creativity [62]. Since the observation of fishes’ natural behaviour is rare compared to other vertebrates, and a generic definition of play applicable throughout Fish are an ideal group to test ecological and evolutionary the animal kingdom has been controversial, early claims of play in links to social cognition. Most species differ in social and/ fish have largely been dismissed [63]. However, Burghardt and col- or ecological complexity in the wild, and we can easily leagues have recently proposed a ‘five criteria’ definition of play that manipulate their social experiences or information per- can also be applied to fish, amphibians and reptiles [62,63], and have reported a peculiar thermometer-striking behaviour in cichlid fish that ception in the laboratory to disentangle some of these fits the play definition [64]. Because of the diversity and sophistica- interactions (e.g. [23,24]). Moreover, we know the biolog- tion of behaviours and cognitive abilities of fishes, it seems only ical functions and metabolic needs driving many social reasonable to assume play behaviour also occurs in fish and thus behaviours are highly conserved across vertebrates, as are should be further investigated. neuromolecular pathways and neural circuits for social decision making [25–27]. Armed with this recent www.sciencedirect.com Current Opinion in Behavioral Sciences 2017, 16:46–52 48 Mixed emotions knowledge, now is an exciting time to study fish social ecological cognition hypothesis [41]. The theory poses cognition using comparative approaches. that the learning and memory skills of an animal are sharply honed by the selective pressures operating in a Similar to humans and other primates, fishes’ social species microhabitat. In a series of papers, White and behaviour and decision-making processes are linked to Brown compared the spatial learning ability of intertidal molecular and gene expression changes (e.g. [28 ,29,30]). gobies from sandy shores versus rocky reefs ([42–44,45 ]; For example, the decision to cooperate or cheat and the Figure 2). Gobies from stable rocky shores need to have perception of reward in cleaner wrasses is modulated by great spatial learning abilities to ensure they return to the cortisol, dopamine and the neuropeptide arginine-vaso- home pool at each low tide to avoid being stranded. tocin [31–33], that are also involved in similar behaviours Gobies from sandy shores, by contrast, need only retreat in monkeys [34].
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