Marine Cleaning Mutualism Defies Standard Logic of Supply and Demand.

AbstractSupply and demand affect the values of goods exchanged in cooperative trades. Studies of humans and other species typically describe the standard scenario that an increase in demand leads to a higher price. Here, we challenge the generality of that logic with empirical data and a theoretical model. In our study system, "client" fishes visit cleaner wrasse (Labroides dimidiatus) to have ectoparasites removed, but cleaners prefer client mucus, which constitutes "cheating." We removed 31 of 65 preselected cleaners from a large isolated reef patch. We compared cleaner-client interactions at the reef and a control reef before removal and 4 weeks after removal. Cleaner fish from the experimental treatment site interacted more frequently with large clients (typically visitors with access to alternative cleaning stations), but we did not observe any changes in service quality measures. A game-theoretic analysis revealed that interaction duration and service quality might increase, decrease, or remain unchanged depending on the precise relationships between key parameters, such as the marginal benefits of cheating as a function of satiation or the likelihood of clients responding to cheating as a function of market conditions. The analyses show that the principle of diminishing return may affect exchanges in ways not predicted by supply-to-demand ratios.

Brain morphology correlates of learning and cognitive flexibility in a fish species (Poecilia reticulata).

Determining how variation in brain morphology affects cognitive abilities is important to understand inter-individual variation in cognition and, ultimately, cognitive evolution. Yet, despite many decades of research in this area, there is surprisingly little experimental data available from assays that quantify cognitive abilities and brain morphology in the same individuals. Here, we tested female guppies (Poecilia reticulata) in two tasks, colour discrimination and reversal learning, to evaluate their learning abilities and cognitive flexibility. We then estimated the size of five brain regions (telencephalon, optic tectum, hypothalamus, cerebellum and dorsal medulla), in addition to relative brain size. We found that optic tectum relative size, in relation to the rest of the brain, correlated positively with discrimination learning performance, while relative telencephalon size correlated positively with reversal learning performance. The other brain measures were not associated with performance in either task. By evaluating how fast learning occurs and how fast an animal adjusts its learning rules to changing conditions, we find support for that different brain regions have distinct functional correlations at the individual level. Importantly, telencephalon size emerges as an important neural correlate of higher executive functions such as cognitive flexibility. This is rare evidence supporting the theory that more neural tissue in key brain regions confers cognitive benefits.

A Farewell to the Encephalization Quotient: A New Brain Size Measure for Comparative Primate Cognition.

Both absolute and relative brain sizes vary greatly among and within the major vertebrate lineages. Scientists have long debated how larger brains in primates and hominins translate into greater cognitive performance, and in particular how to control for the relationship between the noncognitive functions of the brain and body size. One solution to this problem is to establish the slope of cognitive equivalence, i.e., the line connecting organisms with an identical bauplan but different body sizes. The original approach to estimate this slope through intraspecific regressions was abandoned after it became clear that it generated slopes that were too low by an unknown margin due to estimation error. Here, we revisit this method. We control for the error problem by focusing on highly dimorphic primate species with large sample sizes and fitting a line through the mean values for adult females and males. We obtain the best estimate for the slope of circa 0.27, a value much lower than those constructed using all mammal species and close to the value expected based on the genetic correlation between brain size and body size. We also find that the estimate of cognitive brain size based on cognitive equivalence fits empirical cognitive studies better than the encephalization quotient, which should therefore be avoided in future studies on primates and presumably mammals and birds in general. The use of residuals from the line of cognitive equivalence may change conclusions concerning the cognitive abilities of extant and extinct primate species, including hominins.

Relative Brain Size and Cognitive Equivalence in Fishes.

Scientists have long struggled to establish how larger brains translate into higher cognitive performance across species. While absolute brain size often yields high predictive power of performance, its positive correlation with body size warrants some level of correction. It is expected that larger brains are needed to control larger bodies without any changes in cognitive performance. Potentially, the mean value of intraspecific brain-body slopes provides the best available estimate for an interspecific correction factor. For example, in primates, including humans, an increase in body size translates into an increase in brain size without changes in cognitive performance. Here, we provide the first evaluation of this hypothesis for another clade, teleost fishes. First, we obtained a mean intraspecific brain-body regression slope of 0.46 (albeit with a relatively large range of 0.26-0.79) from a dataset of 51 species, with at least 10 wild adult specimens per species. This mean intraspecific slope value (0.46) is similar to that of the encephalisation quotient reported for teleosts (0.5), which can be used to predict mean cognitive performance in fishes. Importantly, such a mean value (0.46) is much higher than in endothermic vertebrate species (≤0.3). Second, we used wild-caught adult cleaner fish Labroides dimidiatus as a case study to test whether variation in individual cognitive performance can be explained by body size. We first obtained the brain-body regression slope for this species from two different datasets, which gave slope values of 0.58 (MRI scan data) and 0.47 (dissection data). Then, we used another dataset involving 69 adult cleaners different from those tested for their brain-body slope. We found that cognitive performance from four different tasks that estimated their learning, numerical, and inhibitory control abilities was not significantly associated with body size. These results suggest that the intraspecific brain-body slope captures cognitive equivalence for this species. That is, individuals that are on the brain-body regression line are cognitively equal. While rather preliminary, our results suggest that fish and mammalian brain organisations are fundamentally different, resulting in different intra- and interspecific slopes of cognitive equivalence.

The impact of long-term reduced access to cleaner fish on health indicators of resident client fish.

In many mutualisms, benefits in the form of food are exchanged for services such as transport or protection. In the marine cleaning mutualism, a variety of 'client' reef fishes offer 'cleaner' fish Labroides dimidiatus access to food in the form of their ectoparasites, where parasite removal supposedly protects the clients. Yet, the health benefits individual clients obtain in the long term from repeated ectoparasite removal remain relatively unknown. Here, we tested whether long-term reduced access to cleaning services alters indicators of health status such as body condition, immunity and the steroids cortisol and testosterone in four client damselfish species Pomacentrus amboinensis, Amblyglyphidodon curacao, Acanthochromis polyacanthus and Dischistodus perspicillatus To do so, we took advantage of a long-term experimental project in which several small reefs around Lizard Island (Great Barrier Reef, Australia) have been maintained cleaner-free since the year 2000, while control reefs had their cleaner presence continuously monitored. We found that the four damselfish species from reef sites without cleaners for 13 years had lower body condition than fish from reefs with cleaners. However, immunity measurements and cortisol and testosterone levels did not differ between experimental groups. Our findings suggest that clients use the energetic benefits derived from long-term access to cleaning services to selectively increase body condition, rather than altering hormonal or immune system functions.

Population densities predict forebrain size variation in the cleaner fish Labroides dimidiatus.

The 'social brain hypothesis' proposes a causal link between social complexity and either brain size or the size of key brain parts known to be involved in cognitive processing and decision-making. While previous work has focused on comparisons between species, how social complexity affects plasticity in brain morphology at the intraspecific level remains mostly unexplored. A suitable study model is the mutualist 'cleaner' fish Labroides dimidiatus, a species that removes ectoparasites from a variety of 'client' fishes in iterative social interactions. Here, we report a positive relationship between the local density of cleaners, as a proxy of both intra- and interspecific sociality, and the size of the cleaner's brain parts suggested to be associated with cognitive functions, such as the diencephalon and telencephalon (that together form the forebrain). In contrast, the size of the mesencephalon, rhombencephalon, and brain stem, assumed more basal in function, were independent of local fish densities. Selective enlargement of brain parts, that is mosaic brain adjustment, appears to be driven by population density in cleaner fish.

Endogenous oxytocin predicts helping and conversation as a function of group membership.

Humans cooperate with unrelated individuals to an extent that far outstrips any other species. We also display extreme variation in decisions about whether to cooperate or not, and the mechanisms driving this variation remain an open question across the behavioural sciences. One candidate mechanism underlying this variation in cooperation is the evolutionary ancient neurohormone oxytocin (OT). As current research focuses on artificial administration of OT in asocial tasks, little is known about how the hormone in its naturally occurring state actually impacts behaviour in social interactions. Using a new optimal foraging paradigm, the 'egg hunt', we assessed the association of endogenous OT with helping behaviour and conversation. We manipulated players' group membership relative to each other prior to an egg hunt, during which they had repeated opportunities to spontaneously help each other. Results show that endogenous baseline OT predicted helping and conversation type, but crucially as a function of group membership. Higher baseline OT predicted increased helping but only between in-group players, as well as decreased discussion about individuals' goals between in-group players but conversely more of such discussion between out-group players. Subsequently, behaviour but not conversation during the hunt predicted change in OT, in that out-group members who did not help showed a decrease in OT from baseline levels. In sum, endogenous OT predicts helping behaviour and conversation, importantly as a function of group membership, and this effect occurs in parallel to uniquely human cognitive processes.

A decrease in the abundance and strategic sophistication of cleaner fish after environmental perturbations.

Coral reef ecosystems are declining worldwide and under foreseeable threat due to climate change, resulting in significant changes in reef communities. It is unknown, however, how such community changes impact interspecific interactions. Recent extreme weather events affecting the Great Barrier Reef, that is, consecutive cyclones and the 2016 El Niño event, allowed us to explore potential consequences in the mutualistic interactions involving cleaner fish Labroides dimidiatus (hereafter "cleaner"). After the perturbations, cleaner densities were reduced by 80%, disproportionally compared to the variety of reef fish clients from which cleaners remove ectoparasites. Consequently, shifts in supply and demand yielded an increase in the clients' demand for cleaning. Therefore, clients became less selective toward cleaners, whereas cleaners were able to choose from a multitude of partners. In parallel, we found a significant decline in the ability of cleaners to manage their reputation and to learn to prioritize ephemeral food sources to maximize food intake in laboratory experiments. In other words, cleaners failed to display the previously documented strategic sophistication that made this species a prime example for fish intelligence. In conclusion, low population densities may cause various effects on individual behavior, and as a consequence, interspecific interactions. At the same time, our data suggest that a recovery of population densities would cause a recovery of previously described interaction patterns and cleaner strategic sophistication within the lifetime of individuals.

Cleaner fish Labroides dimidiatus discriminate numbers but fail a mental number line test.

Several species of primates, including humans, possess a spontaneous spatial mental arrangement (i.e. mental number line MNL) of increasing numbers or continuous quantities from left to right. This cognitive process has recently been documented in domestic chicken in a spatial-numerical task, opening the possibility that MNL is a cognitive capacity that has been conserved across vertebrate taxa. In this scenario, fish might possess the MNL as well. Here we investigated whether cleaner fish Labroides dimidiatus show evidence for MNL in two experiments. In Experiment I, we tested fish's abilities in number discrimination, presenting simultaneously either small (2 vs 5) or large (5 vs 8) continuous quantities where one quantity was systematically rewarded. Experiment II used a protocol of an MNL task similar to the study on chickens. We trained cleaners with a target number (i.e. 5 elements), then we presented them with an identical pair of panels depicting either 2 elements or 8 elements, and we recorded their spontaneous choice for the left or right panel on each presentation. Cleaner fish showed high abilities in discriminating small and large numbers in Experiment I. Importantly, cleaners achieved this discrimination using numerical cues instead of non-numerical cues such as the cumulative surface area, density, and overall space. In contrast, cleaners did not allocate continuous quantities to space in Experiment II. Our findings suggest that cleaner fish possess numbering skills but they do not have an MNL. While similar studies on animals from various clades are needed to trace the evolution of MNL within vertebrates, our results suggest that this cognitive process might not be a capacity conserved across all vertebrate taxa.

A Role for Oxytocin-Like Receptor in Social Habituation in a Teleost.

Oxytocin (OT) mediates social habituation in rodent model systems, but its role in mediating this effect in other vertebrates is unknown. We used males of the African cichlid fish, Astatotilapia burtoni, to investigate two aspects of isotocin (IT; an OT homolog) signaling in social habituation. First, we examined the expression of IT receptor 2 (ITR2) as well as two immediate early genes in brain regions implicated in social recognition. Next, we examined IT neuron activity using immunohistochemistry. Patterns of gene expression in homologs of the amygdala and hippocampus implicate IT signaling in these regions in social habituation to a territorial neighbor. In the preoptic area, the expression of the ITR2 subtype and IT neuron activity respond to the presence of a male, independent of familiarity. Our results implicate IT in mediating social habituation in a teleost.

Executive functions and brain morphology of male and female dominant and subordinate cichlid fish.

BACKGROUND: Living in a social dominance hierarchy presents different benefits and challenges for dominant and subordinate males and females, which might in turn affect their cognitive needs. Despite the extensive research on social dominance in group-living species, there is still a knowledge gap regarding how social status impacts brain morphology and cognitive abilities. METHODS: Here, we tested male and female dominants and subordinates of Neolamprologus pulcher, a social cichlid fish species with size-based hierarchy. We ran three executive cognitive function tests for cognitive flexibility (reversal learning test), self-control (detour test), and working memory (object permanence test), followed by brain and brain region size measurements. RESULTS: Performance was not influenced by social status or sex. However, dominants exhibited a brain-body slope that was relatively steeper than that of subordinates. Furthermore, individual performance in reversal learning and detour tests correlated with brain morphology, with some trade-offs among major brain regions like telencephalon, cerebellum, and optic tectum. CONCLUSION: As individuals' brain growth strategies varied depending on social status without affecting executive functions, the different associated challenges might yield a potential effect on social cognition instead. Overall, the findings highlight the importance of studying the individual and not just species to understand better how the individual's ecology might shape its brain and cognition.

The serotonin blocker Ketanserin reduces coral reef fish Ctenochaetus striatus aggressive behaviour during between-species social interactions.

A multitude of species engages in social interactions not only with their conspecifics but also with other species. Such interspecific interactions can be either positive, like helping, or negative, like aggressive behaviour. However, the physiological mechanisms of these behaviours remain unclear. Here, we manipulated the serotonin system, a well-known neurohormone for regulating intraspecific aggressive behaviour, to investigate its role in interspecific aggression. We tested whether serotonin blockade affects the aggressive behaviour of a coral reef fish species (Ctenochaetus striatus) that engages in mutualistic interactions with another species, the cleaner fish (Labroides dimidiatus). Although this mutualistic cleaning relationship may appear positive, cleaner fish do not always cooperate and remove ectoparasites from the other coral reef fish ("clients") but tend to cheat and bite the client's protective layer of mucus. Client fish thus often apply control mechanisms, like chasing, to deter their cleaner fish partners from cheating. Our findings show that blocking serotonin receptors 5-HT2A and 5-HT2C with ketanserin reduced the client fish's aggressive behaviour towards cleaner fish, but in the context where the latter did not cheat. These results are evidence of the involvement of serotonin in regulating aggressive behaviour at the between-species social interactions level. Yet, the direction of effect we found here is the opposite of previous findings using a similar experimental set-up and ecological context but with a different client fish species (Scolopsis bilineatus). Together, it suggests that serotonin's role in aggressive behaviour is complex, and at least in this mutualistic ecological context, its function is species-dependent. This warrants, to some extent, careful interpretations from single-species studies looking into the physiological mechanisms of social behaviour.

Social complexity affects cognitive abilities but not brain structure in a Poeciliid fish.

Some cognitive abilities are suggested to be the result of a complex social life, allowing individuals to achieve higher fitness through advanced strategies. However, most evidence is correlative. Here, we provide an experimental investigation of how group size and composition affect brain and cognitive development in the guppy (Poecilia reticulata). For 6 months, we reared sexually mature females in one of 3 social treatments: a small conspecific group of 3 guppies, a large heterospecific group of 3 guppies and 3 splash tetras (Copella arnoldi)-a species that co-occurs with the guppy in the wild, and a large conspecific group of 6 guppies. We then tested the guppies' performance in self-control (inhibitory control), operant conditioning (associative learning), and cognitive flexibility (reversal learning) tasks. Using X-ray imaging, we measured their brain size and major brain regions. Larger groups of 6 individuals, both conspecific and heterospecific groups, showed better cognitive flexibility than smaller groups but no difference in self-control and operant conditioning tests. Interestingly, while social manipulation had no significant effect on brain morphology, relatively larger telencephalons were associated with better cognitive flexibility. This suggests alternative mechanisms beyond brain region size enabled greater cognitive flexibility in individuals from larger groups. Although there is no clear evidence for the impact on brain morphology, our research shows that living in larger social groups can enhance cognitive flexibility. This indicates that the social environment plays a role in the cognitive development of guppies.

Experimental expansion of relative telencephalon size improves the main executive function abilities in guppy.

Executive functions are a set of cognitive control processes required for optimizing goal-directed behavior. Despite more than two centuries of research on executive functions, mostly in humans and nonhuman primates, there is still a knowledge gap in what constitutes the mechanistic basis of evolutionary variation in executive function abilities. Here, we show experimentally that size changes in a forebrain structure (i.e. telencephalon) underlie individual variation in executive function capacities in a fish. For this, we used male guppies (Poecilia reticulata) issued from artificial selection lines with substantial differences in telencephalon size relative to the rest of the brain. We tested fish from the up- and down-selected lines not only in three tasks for the main core executive functions: cognitive flexibility, inhibitory control, and working memory, but also in a basic conditioning test that does not require executive functions. Individuals with relatively larger telencephalons outperformed individuals with smaller telencephalons in all three executive function assays but not in the conditioning assay. Based on our findings, we propose that the telencephalon is the executive brain in teleost fish. Together, it suggests that selective enlargement of key brain structures with distinct functions, like the fish telencephalon, is a potent evolutionary pathway toward evolutionary enhancement of advanced cognitive abilities in vertebrates.

Oxytocin has 'tend-and-defend' functionality in group conflict across social vertebrates.

Across vertebrate species, intergroup conflict confronts individuals with a tension between group interests best served by participation in conflict and personal interest best served by not participating. Here, we identify the neurohormone oxytocin as pivotal to the neurobiological regulation of this tension in distinctly different group-living vertebrates, including fishes, birds, rodents, non-human primates and humans. In the context of intergroup conflict, a review of emerging work on pro-sociality suggests that oxytocin and its fish and birds homologues, isotocin and mesotocin, respectively, can elicit participation in group conflict and aggression. This is because it amplifies (i) concern for the interests of genetically related or culturally similar 'in-group' others and (ii) willingness to defend against outside intruders and enemy conspecifics. Across a range of social vertebrates, oxytocin can induce aggressive behaviour to 'tend-and-defend' the in-group during intergroup contests. This article is part of the theme issue 'Intergroup conflict across taxa'.

Intergroup conflict: origins, dynamics and consequences across taxa.

Although uniquely destructive and wasteful, intergroup conflict and warfare are not confined to humans. They are seen across a range of group-living species, from social insects, fishes and birds to mammals, including nonhuman primates. With its unique collection of theory, research and review contributions from biology, anthropology and economics, this theme issue provides novel insights into intergroup conflict across taxa. Here, we introduce and organize this theme issue on the origins and consequences of intergroup conflict. We provide a coherent framework by modelling intergroup conflicts as multi-level games of strategy in which individuals within groups cooperate to compete with (individuals in) other groups for scarce resources, such as territory, food, mating opportunities, power and influence. Within this framework, we identify cross-species mechanisms and consequences of (participating in) intergroup conflict. We conclude by highlighting crosscutting innovations in the study of intergroup conflict set forth by individual contributions. These include, among others, insights on how within-group heterogeneities and leadership relate to group conflict, how intergroup conflict shapes social organization and how climate change and environmental degradation transition intergroup relations from peaceful coexistence to violent conflict. This article is part of the theme issue 'Intergroup conflict across taxa'.

Artificial mosaic brain evolution of relative telencephalon size improves inhibitory control abilities in the guppy (Poecilia reticulata).

Mosaic brain evolution, the change in the size of separate brain regions in response to selection on cognitive performance, is an important idea in the field of cognitive evolution. However, untill now, most of the data on how separate brain regions respond to selection and their cognitive consequences stem from comparative studies. To experimentally investigate the influence of mosaic brain evolution on cognitive ability, we used male guppies artificially selected for large and small telencephalons relative to the rest of the brain. Here, we tested an important aspect of executive cognitive ability using a detour task. We found that males with larger telencephalons outperformed males with smaller telencephalons. Fish with larger telencephalons showed faster improvement in performance during detour training and were more successful in reaching the food reward without touching the transparent barrier (i.e., through correct detouring) during the test phase. Together, our findings provide the first experimental evidence showing that evolutionary enlargement of relative telencephalon size confers cognitive benefits, supporting an important role for mosaic brain evolution during cognitive evolution.

Sex differences in the cognitive abilities of a sex-changing fish species Labroides dimidiatus.

Males and females of the same species are known to differ at least in some cognitive domains, but such differences are not systematic across species. As a consequence, it remains unclear whether reported differences generally reflect adaptive adjustments to diverging selective pressures, or whether differences are mere side products of physiological differences necessary for reproduction. Here, we show that sex differences in cognition occur even in a sex-changing species, a protogynous hermaphroditic species where all males have previously been females. We tested male and female cleaner fish Labroides dimidiatus in four cognitive tasks to evaluate their learning and inhibitory control abilities first in an abstract presentation of the tasks, then in more ecologically relevant contexts. The results showed that males were better learners than females in the two learning tasks (i.e. reversal learning as an abstract task and a food quantity assessment task as an ecologically relevant task). Conversely, females showed enhanced abilities compared with males in the abstract inhibitory control task (i.e. detour task); but both sexes performed equally in the ecologically relevant inhibitory control task (i.e. 'audience effect' task). Hence, sex-changing species may offer unique opportunities to study proximate and/or ultimate causes underlying sex differences in cognitive abilities.

Brain morphology predicts social intelligence in wild cleaner fish.

It is generally agreed that variation in social and/or environmental complexity yields variation in selective pressures on brain anatomy, where more complex brains should yield increased intelligence. While these insights are based on many evolutionary studies, it remains unclear how ecology impacts brain plasticity and subsequently cognitive performance within a species. Here, we show that in wild cleaner fish (Labroides dimidiatus), forebrain size of high-performing individuals tested in an ephemeral reward task covaried positively with cleaner density, while cerebellum size covaried negatively with cleaner density. This unexpected relationship may be explained if we consider that performance in this task reflects the decision rules that individuals use in nature rather than learning abilities: cleaners with relatively larger forebrains used decision-rules that appeared to be locally optimal. Thus, social competence seems to be a suitable proxy of intelligence to understand individual differences under natural conditions.

Fluctuations in coral reef fish densities after environmental disturbances on the northern Great Barrier Reef.

Global warming is predicted to increase the frequency and or severity of many disturbances including cyclones, storms, and prolonged heatwaves. The coral reef at Lizard Island, part of the Great Barrier Reef, has been recently exposed to a sequence of severe tropical cyclones (i.e., Ita in 2014 and Nathan in 2015) and a coral bleaching in the year 2016. Reef fishes are an essential part of the coral reef ecosystem, and their abundance is thus a good marker to estimate the magnitude of such disturbances. Here, we examined whether the recent disturbances at Lizard Island had an impact on the coral reef fish communities. To do this, we examined fish survey data collected before and after the disturbances for potential changes in total fish density post-disturbance. Also, by sorting fish species into 11 functional groups based on their trophic level (i.e., diet), we further explored the density changes within each functional group. Our findings showed an overall decline of 68% in fish density post-disturbance, with a significant density decrease in nine of 11 trophic groups. These nine groups were: browsers, corallivores, detritivores, excavator/scrapers, grazers, macro-invertivores, pisci-invertivores, planktivores, and spongivores. The piscivores, on the other hand, were the only "winners," wherein their density showed an increase post-disturbance. These changes within functional groups might have a further impact on the trophodynamics of the food web. In summary, our findings provide evidence that the fish assemblage on the reefs around Lizard Island was considerably affected by extreme weather events, leading to changes in the functional composition of the reef fish assemblage.