Social bond dynamics and the evolution of helping.

Empiricists often struggle to apply game theory models to real-life cases of animal cooperation. One reason is that many examples of cooperation occur in stable groups, where individuals form social bonds that influence exchanges of help in ways that are not well described by previous models, including the extent of reciprocity and how relationships are initiated. We present a game theory model exploring the conditions under which social bonds between group members promote cooperation. In the model, bonds build up from exchanges of help in a similar way as the strength of association increases in learning, as in the Rescorla-Wagner rule. The bonds in turn affect partner choice and influence helping amounts. The model has a mechanism of reciprocity for bonded pairs, which can evolve toward either loose or strict reciprocation. Several aspects of the model are inspired by observations of food sharing in vampire bats. We find that small social neighborhoods are required for the evolutionary stability of helping, either as small group sizes, or if bonded members of larger groups can form temporary (daily) smaller groupings. The costs of helping need to be fairly low, while the benefits can be substantial. The form of reciprocity that evolves is neither immediate nor very strict. Individuals in need request help based on bond strength, but there is also an evolved preference for initiating bonds with new group members. In contrast, if different groups come into temporary contact, the evolved tendency is to avoid forming bonds between groups.

Cleaner fish recognize self in a mirror via self-face recognition like humans.

Some animals have the remarkable capacity for mirror self-recognition (MSR), yet any implications for self-awareness remain uncertain and controversial. This is largely because explicit tests of the two potential mechanisms underlying MSR are still lacking: mental image of the self and kinesthetic visual matching. Here, we test the hypothesis that MSR ability in cleaner fish, Labroides dimidiatus, is associated with a mental image of the self, in particular the self-face, like in humans. Mirror-naive fish initially attacked photograph models of both themselves and unfamiliar strangers. In contrast, after all fish had passed the mirror mark test, fish did not attack their own (motionless) images, but still frequently attacked those of unfamiliar individuals. When fish were exposed to composite photographs, the self-face/unfamiliar body were not attacked, but photographs of unfamiliar face/self-body were attacked, demonstrating that cleaner fish with MSR capacity recognize their own facial characteristics in photographs. Additionally, when presented with self-photographs with a mark placed on the throat, unmarked mirror-experienced cleaner fish demonstrated throat-scraping behaviors. When combined, our results provide clear evidence that cleaner fish recognize themselves in photographs and that the likely mechanism for MSR is associated with a mental image of the self-face, not a kinesthetic visual-matching model. Humans are also capable of having a mental image of the self-face, which is considered an example of private self-awareness. We demonstrate that combining mirror test experiments with photographs has enormous potential to further our understanding of the evolution of cognitive processes and private self-awareness across nonhuman animals.

Modelling how cleaner fish approach an ephemeral reward task demonstrates a role for ecologically tuned chunking in the evolution of advanced cognition.

What makes cognition "advanced" is an open and not precisely defined question. One perspective involves increasing the complexity of associative learning, from conditioning to learning sequences of events ("chaining") to representing various cue combinations as "chunks." Here we develop a weighted graph model to study the mechanism enabling chunking ability and the conditions for its evolution and success, based on the ecology of the cleaner fish Labroides dimidiatus. In some environments, cleaners must learn to serve visitor clients before resident clients, because a visitor leaves if not attended while a resident waits for service. This challenge has been captured in various versions of the ephemeral reward task, which has been proven difficult for a range of cognitively capable species. We show that chaining is the minimal requirement for solving this task in its common simplified laboratory format that involves repeated simultaneous exposure to an ephemeral and permanent food source. Adding ephemeral-ephemeral and permanent-permanent combinations, as cleaners face in the wild, requires individuals to have chunking abilities to solve the task. Importantly, chunking parameters need to be calibrated to ecological conditions in order to produce adaptive decisions. Thus, it is the fine-tuning of this ability, which may be the major target of selection during the evolution of advanced associative learning.

Further evidence for the capacity of mirror self-recognition in cleaner fish and the significance of ecologically relevant marks.

An animal that tries to remove a mark from its body that is only visible when looking into a mirror displays the capacity for mirror self-recognition (MSR), which has been interpreted as evidence for self-awareness. Conservative interpretations of existing data conclude that convincing evidence for MSR is currently restricted to great apes. Here, we address proposed shortcomings of a previous study on MSR in the cleaner wrasse Labroides dimidiatus, by varying preexposure to mirrors and by marking individuals with different colors. We found that (1) 14/14 new individuals scraped their throat when a brown mark had been provisioned, but only in the presence of a mirror; (2) blue and green color marks did not elicit scraping; (3) intentionally injecting the mark deeper beneath the skin reliably elicited spontaneous scraping in the absence of a mirror; (4) mirror-naive individuals injected with a brown mark scraped their throat with lower probability and/or lower frequency compared to mirror-experienced individuals; (5) in contrast to the mirror images, seeing another fish with the same marking did not induce throat scraping; and (6) moving the mirror to another location did not elicit renewed aggression in mirror-experienced individuals. Taken together, these results increase our confidence that cleaner fish indeed pass the mark test, although only if it is presented in ecologically relevant contexts. Therefore, we reiterate the conclusion of the previous study that either self-awareness in animals or the validity of the mirror test needs to be revised.

Oxytocin and shared intentionality are positively associated with cooperation in children.

While 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. A diversity of cognitive, affective, social, and physiological mechanisms interact to shape these decisions. For example, group membership, shared intentionality talk (i.e. talk about shared goals), and natural initial oxytocin levels are linked to cooperation in adults in an optimal foraging paradigm that is loosely modelled on the iterated prisoner's dilemma. In this 'egg hunt', shared intentionality talk was key to achieving cooperation, and it drove cooperation more between participants who shared the same group membership (and who also had higher initial oxytocin levels). Such complex interactions raise the question of the age at which humans develop the necessary mechanisms to cooperate effectively in the egg hunt game. Here, we tested children in secondary school aged between 10 and 14 years. We found that, as for adults, shared intentionality talk was crucial for successful cooperation. Furthermore, initial oxytocin levels correlated with cooperation through shared intentionality talk. In contrast, group membership did not affect behaviour. Finally, pre- and post-experiment oxytocin levels showed various interactions with group membership and sex. Thus, children's performance was relatively similar to adults while showing some differences with respect to underlying mechanisms. Our study is a rare contribution to further our understanding of the role of oxytocin in early adolescent social behaviour.

Comparative Brain Morphology of Cleaning and Sponge-Dwelling Elacatinus Gobies.

INTRODUCTION: Comparative studies of brain anatomy between closely related species have been very useful in demonstrating selective changes in brain structure. Within-species comparisons can be particularly useful for identifying changes in brain structure caused by contrasting environmental selection pressures. Here, we aimed to understand whether differences within and between species in habitat use and foraging behaviour influence brain morphology, on both ecological and evolutionary time scales. METHODS: We used as a study model three species of the Elacatinus genus that differ in their habitat-foraging mode. The obligatory cleaning goby Elacatinus evelynae inhabits mainly corals and feeds mostly on ectoparasites removed from larger fish during cleaning interactions. In contrast, the obligatory sponge-dwelling goby Elacatinus chancei inhabits tubular sponges and feeds on microinvertebrates buried in the sponges' tissues. Finally, in the facultatively cleaning goby Elacatinus prochilos, individuals can adopt either phenotype, the cleaning or the sponge-dwelling habitat-foraging mode. By comparing the brains of the facultative goby phenotypes to the brains of the obligatory species we can test whether brain morphology is better predicted by phylogenetic relatedness or the habitat-foraging modes (cleaning × sponge dwelling). RESULTS: We found that E. prochilos brains from both types (cleaning and sponge dwelling) were highly similar to each other. Their brains were in general more similar to the brains of the most closely related species, E. evelynae (obligatory cleaning species), than to the brains of E. chancei (sponge-dwelling species). In contrast, we found significant brain structure differences between the cleaning species (E. evelynae and E. prochilos) and the sponge-dwelling species (E. chancei). These differences revealed independent changes in functionally correlated brain areas that might be ecologically adaptive. E. evelynae and E. prochilos had a relatively larger visual input processing brain axis and a relatively smaller lateral line input processing brain axis than E. chancei. CONCLUSION: The similar brain morphology of the two types of E. prochilos corroborates other studies showing that individuals of both types can be highly plastic in their social and foraging behaviours. Our results in the Elacatinus species suggest that morphological adaptations of the brain are likely to be found in specialists whereas species that are more flexible in their habitat may only show behavioural plasticity without showing anatomical differences.

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.

Effects of local versus global competition on reproductive skew and sex differences in social dominance behaviour.

Social hierarchies are often found in group-living animals. The hierarchy position can influence reproductive success (RS), with a skew towards high-ranking individuals. The amount of aggression in social dominance varies greatly, both between species and between males and females within species. Using game theory we study this variation by taking into account the degree to which reproductive competition in a social group is mainly local to the group, emphasizing within-group relative RS, or global to a larger population, emphasizing an individual's absolute RS. Our model is similar to recent approaches in that reinforcement learning is used as a behavioural mechanism allowing social-hierarchy formation. We test two hypotheses. The first is that local competition should favour the evolution of mating or foraging interference, and thus of reproductive skew. Second, decreases in reproductive output caused by an individual's accumulated fighting damage, such as reduced parenting ability, will favour less intense aggression but should have little influence on reproductive skew. From individual-based simulations of the evolution of social dominance and interference, we find support for both hypotheses. We discuss to what extent our results can explain observed sex differences in reproductive skew and social dominance behaviour.

Reproductive skew, fighting costs and winner-loser effects in social dominance evolution.

Social hierarchies are often found in group-living animals and can be formed through pairwise aggressive interactions. The dominance rank can influence reproductive success (RS) with a skew towards high-ranking individuals. Using game theory, we investigate how the opportunity for differently ranked individuals to achieve RS influences the costs of hierarchy formation and the strength of winner and loser effects. In our model, individuals adjust their aggressive and submissive behaviour towards others through reinforcement learning. The learning is based on rewards and penalties, which depend on relative fighting ability. From individual-based simulations, we determine evolutionary equilibria of traits such as learning rates. We examine situations that differ in the extent of monopolisation of contested RS by dominants and in the proportion of total RS that is contested. The model implements two kinds of fighting costs: a decrease in effective fighting ability from damage (loss of condition) and a risk of mortality that increases with the total accumulated damage. Either of these costs can limit the amount of fighting. We find that individuals form stable dominance hierarchies, with a positive correlation between dominance position and fighting ability. The accumulated costs differ between dominance positions, with the highest costs paid by low or intermediately ranked individuals. Costs tend to be higher in high-skew situations. We identify a 'stay-in, opt-out' syndrome, comprising a range from weaker (stay-in) to stronger (opt-out) winner-loser effects. We interpret the opt-out phenotype to be favoured by selection on lower ranked individuals to opt out of contests over social dominance, because it is more pronounced when more of the total RS is uncontested. We discuss our results in relation to field and experimental observations and argue that there is a need for empirical investigation of the behaviour and reproductive success of lower ranked individuals.

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.

Comparative performance of orangutans (Pongo spp.), gorillas (Gorilla gorilla gorilla), and drills (Mandrillus leucophaeus), in an ephemeral foraging task.

A goal of the comparative approach is to test a variety of species on the same task. Here, we examined whether the factors that helped capuchin monkeys improve their performance in a dichotomous choice task would generalize to three other primate species: orangutans, gorillas, and drill monkeys. In this task, subjects have access to two options, each resulting in an identical food, but one (the ephemeral option) is only available if it is chosen first, whereas the other one (the permanent option) is always available. Therefore, the food-maximizing solution is to choose the ephemeral option first, followed by the permanent option for an additional reward. On the original version (plate task), the options were discriminated by the color and pattern of the plates holding the food, while on two subsequent versions we used altered cues that we predicted would improve performance: (1) the color of the foods themselves (color task), which we hypothesized was relevant to primates, who choose foods rather than substrates on which foods are found when foraging, and (2) patterned cups covering the foods (cup task), which we hypothesized would help primates avoid the prepotent response associated with visible food. Like capuchins, all three species initially failed to solve the plate task. However, while orangutans improved their performance from the plate to the color task, they did not for the cup task, and only a few gorillas and no drills succeeded in either task. Unfortunately, our ability to interpret these data was obscured by differences in the subjects' level of experience with cognitive testing and practical constraints that precluded the use of completely identical procedures across species. Nonetheless, we consider what these results can tell us, and discuss the value of conducting studies across multiple sites despite unavoidable differences.

Reinforcement Learning Theory Reveals the Cognitive Requirements for Solving the Cleaner Fish Market Task.

Learning is an adaptation that allows individuals to respond to environmental stimuli in ways that improve their reproductive outcomes. The degree of sophistication in learning mechanisms potentially explains variation in behavioral responses. Here, we present a model of learning that is inspired by documented intra- and interspecific variation in the performance of a simultaneous two-choice task, the biological market task. The task presents a problem that cleaner fish often face in nature: choosing between two client types, one that is willing to wait for inspection and one that may leave if ignored. The cleaner's choice hence influences the future availability of clients (i.e., it influences food availability). We show that learning the preference that maximizes food intake requires subjects to represent in their memory different combinations of pairs of client types rather than just individual client types. In addition, subjects need to account for future consequences of actions, either by estimating expected long-term reward or by experiencing a client leaving as a penalty (negative reward). Finally, learning is influenced by the absolute and relative abundance of client types. Thus, cognitive mechanisms and ecological conditions jointly explain intra- and interspecific variation in the ability to learn the adaptive response.

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.

Ecological differences in the facultative Caribbean cleaning goby Elacatinus prochilos do not predict learning performance in discriminatory two-choice tasks.

The ecological approach to comparative cognition emphasizes that the ecological and social environment are important predictors of cognitive performance. We used this approach to test whether differences in habitat use and social behavior in the facultative Caribbean cleaning goby Elacatinus prochilos predict differences in learning performance in two discriminatory two-choice tasks. This species has two behavioral ecotypes: one that frequently engages in cleaning interactions and inhabits corals in male-female pairs (cleaning gobies) and another that rarely engages in cleaning interactions and inhabits barrel sponges in large groups (sponge-dwellers). We predicted that cleaning gobies would outperform sponge-dwellers in a pattern-cued task, which consisted of identifying the pattern on a plate that consistently provided food, while sponge-dwellers would outperform cleaning gobies in a spatial task, which consisted of identifying the location of the plate. Contrary to our predictions, there was no difference in performance between the two ecotypes. Most of the gobies performed poorly in the pattern-cued task and well in the spatial task. A possible explanation for these results is that the association of a pattern with positive and negative reinforcement may not be a pre-requisite for engaging in cleaning interactions, while spatial skills might be equally required in both ecotypes. Alternatively, the two ecotypes can flexibly adjust to new feeding conditions, which would explain their similar performance in the spatial task. Further research should investigate which aspects of E. prochilos' social and ecological environment might impose challenges that require spatial cognition and whether individuals can flexibly adjust to new habitats and feeding conditions.

The past, present and future of cleaner fish cognitive performance as a function of CO2 levels.

Ocean acidification is one of the many consequences of climate change. Various studies suggest that marine organisms' behaviour will be impaired under high CO2. Here, we show that the cognitive performance of the cleaner wrasse, Labroides dimidiatus, has not suffered from the increase of CO2 from pre-industrial levels to today, and that the standing variation in CO2 tolerance offers potential for adaptation to at least 750 µatm. We acclimated cleaners over 30 days to five levels of pCO2, from pre-industrial to high future CO2 scenarios, before testing them in an ecologically relevant task-the ability to learn to prioritize an ephemeral food source over a permanent one. Fish learning abilities remained stable from pre-industrial to present-day pCO2. While performance was reduced under mid (750 µatm) and high CO2 (980 µatm) scenarios, under the former 36% of cleaners still solved the task. The presence of tolerant individuals reveals potential for adaptation, as long as selection pressure on cognitive performance is strong. However, the apparent absence of high CO2 tolerant fish, and potentially synergistic effects between various climate change stressors, renders the probability of further adaptation unlikely.

Simple decision rules underlie collaborative hunting in yellow saddle goatfish.

Collaborative hunting, the coordination of animal behaviour in space and time to capture prey, is reported in several vertebrate species. However, previous studies are observational, hampering our ability to identify individual decision rules that result in collaboration. We experimentally investigated collaborative hunting in yellow saddle goatfish (Parupeneus cyclostomus) by exposing pairs to a mock prey that fled to an artificial shelter with multiple entrances. The first fish to initiate the chase (the 'initiator') was always closest to the prey and pursued it directly in its path. Conversely, the behaviour of the second goatfish (the 'follower') depended on its spatial position relative to the initiator. When the follower was less than one body length behind the initiator, it also accelerated directly towards the prey in over 95% of cases. However, if the two goatfish were separated by a distance of one body length or more, the follower chose a less direct route to reach the prey in 87% of cases. In this scenario, the follower often reached the prey's more distant refuge first, which might increase its hunting success or block the prey's escape path under natural conditions. Our findings suggest that coordinated hunting behaviour can result from simple, self-serving decisions.

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.

Cleaner wrasse indirectly affect the cognitive performance of a damselfish through ectoparasite removal.

Cleaning organisms play a fundamental ecological role by removing ectoparasites and infected tissue from client surfaces. We used the well-studied cleaning mutualisms involving the cleaner wrasse, Labroides dimidiatus, to test how client cognition is affected by ectoparasites and whether these effects are mitigated by cleaners. Ambon damselfish (Pomacentrus amboinensis) collected from experimental reef patches without cleaner wrasse performed worse in a visual discrimination test than conspecifics from patches with cleaners. Endoparasite abundance also negatively influenced success in this test. Visual discrimination performance was also impaired in damselfish experimentally infected with gnathiid (Crustacea: Isopoda) ectoparasites. Neither cleaner absence nor gnathiid infection affected performance in spatial recognition or reversal learning tests. Injection with immune-stimulating lipopolysaccharide did not affect visual discrimination performance relative to saline-injected controls, suggesting that cognitive impairments are not due to an innate immune response. Our results highlight the complex, indirect role of cleaning organisms in promoting the health of their clients via ectoparasite removal and emphasize the negative impact of parasites on host's cognitive abilities.