Brain morphology predicts social intelligence in wild cleaner fish.
ABSTRACT: 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.
Project description:Predatory reef fishes regularly visit mutualistic cleaner fish (Labroides dimidiatus) to get their ectoparasites removed but show no interest in eating them. The concept of compensated trait loss posits that characters can be lost if a mutualistic relationship reduces the need for a given trait. Thus, selective pressures on escape performance might have relaxed in L. dimidiatus due to its privileged relationship with predators. However, the cost of failing to escape a predatory strike is extreme even if predation events on cleaners are exceptionally rare. Additionally, cleaners must escape from non-predatory clients that regularly punish them for eating mucus instead of parasites. Therefore, strong escape capabilities might instead be maintained in cleaner fish because they must be able to flee when in close proximity to predators or dissatisfied clients. We compared the fast-start escape performance of L. dimidiatus with that of five closely related wrasse species and found that the mutualistic relationship that cleaners entertain with predators has not led to reduced escape performance. Instead, conflicts in cleaning interactions appear to have maintained selective pressures on this trait, suggesting that compensated trait loss might only evolve in cases of high interdependence between mutualistic partners that are not tempted to cheat.
Project description:Accurate contextual decision-making strategies are important in social environments. Specific areas in the brain are tasked to process these complex interactions and generate correct follow-up responses. The dorsolateral and dorsomedial parts of the telencephalon in the teleost fish brain are neural substrates modulated by the neurotransmitter dopamine (DA), and are part of an important neural circuitry that drives animal behaviour from the most basic actions such as learning to search for food, to properly choosing partners and managing decisions based on context. The Indo-Pacific cleaner wrasse Labroides dimidiatus is a highly social teleost fish species with a complex network of interactions with its 'client' reef fish. We asked if changes in DA signalling would affect individual learning ability by presenting cleaner fish two ecologically different tasks that simulated a natural situation requiring accurate decision-making. We demonstrate that there is an involvement of the DA system and D1 receptor pathways on cleaners' natural abilities to learn both tasks. Our results add significantly to the growing literature on the physiological mechanisms that underlie and facilitate the expression of cooperative abilities.
Project description: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.
Project description:Adjusting one's behaviour in response to eavesdropping bystanders is considered a sophisticated social strategy, yet the underlying mechanisms are not well studied. Cleaner wrasse, Labroides dimidiatus, cooperate by eating ectoparasites off "client" fishes, or cheat (i.e. bite) and eat client mucus. Image scoring by bystander clients generally causes cleaners from socially-complex (i.e. high cleaner and client abundance; high client species richness) habitats to increase levels of cooperation. However, some individuals may periodically provide tactile stimulation to small resident clients, which attract bystanders close that are bitten, a form of tactical deception. Cortisol injection can reproduce this pattern. Here, we tested whether cleaners from socially-complex versus simple habitats respond differently to cortisol injections in terms of their cleaning interactions with clients. We found that only cleaners from the socially-complex habitat respond to cortisol injection with strategies functioning as tactical deception: i.e. increased tactile stimulation to small clients and increased cheating of large clients relative to small ones. At the socially-simple site, where reputation management is less important, cortisol-treated fish increased their overall levels of cheating, especially of small clients. Thus, strategic adjustments to cooperative behaviour and tactical deception are likely context-dependent, forming part of general reputation management abilities in cleaner wrasse.
Project description:Social learning is often proposed as an important driver of the evolution of human cooperation. In this view, cooperation in other species might be restricted because it mostly relies on individually learned or innate behaviours. Here, we show that juvenile cleaner fish (Labroides dimidiatus) can learn socially about cheating consequences in an experimental paradigm that mimics cleaners' cooperative interactions with client fish. Juvenile cleaners that had observed adults interacting with model clients learned to (1) behave more cooperatively after observing clients fleeing in response to cheating; (2) prefer clients that were tolerant to cheating; but (3) did not copy adults' arbitrary feeding preferences. These results confirm that social learning can play an active role in the development of cooperative strategies in a non-human animal. They further show that negative responses to cheating can potentially shape the reputation of cheated individuals, influencing cooperation dynamics in interaction networks.
Project description:In many instances of cooperation, only one individual has both the potential and the incentive to 'cheat' and exploit its partner. Under these asymmetric conditions, a simple model predicts that variation in the temptation to cheat and in the potential victim's capacity for partner control leads to shifts between exploitation and cooperation. Here, we show that the threat of early termination of an interaction was sufficient to induce cleaner wrasse Labroides dimidiatus to feed selectively against their preference (which corresponds to cooperatively eating client fish ectoparasites), provided that their preference for alternative food was weak. Under opposite conditions, cleaners fed selectively according to their own preference (which corresponds to cheating by eating client mucus). By contrast, a non-cleaning fish species, Halichoeres melanurus, failed to adjust its foraging behaviour under these same conditions. Thus, cleaners appear to have evolved the power to strategically adjust their levels of cooperation according to the circumstances.
Project description:Mutualisms affect the biodiversity, distribution and abundance of biological communities. However, ecological processes that drive mutualism-related shifts in population structure are often unclear and must be examined to elucidate how complex, multi-species mutualistic networks are formed and structured. In this study, we investigated how the presence of key marine mutualistic partners can drive the organisation of local communities on coral reefs. The cleaner wrasse, Labroides dimidiatus, removes ectoparasites and reduces stress hormones for multiple reef fish species, and their presence on coral reefs increases fish abundance and diversity. Such changes in population structure could be driven by increased recruitment of larval fish at settlement, or by post-settlement processes such as modified levels of migration or predation. We conducted a controlled field experiment to examine the effect of cleaners on recruitment processes of a common group of reef fishes, and showed that small patch reefs (61-285 m(2)) with cleaner wrasse had higher abundances of damselfish recruits than reefs from which cleaner wrasse had been removed over a 12-year period. However, the presence of cleaner wrasse did not affect species diversity of damselfish recruits. Our study provides evidence of the ecological processes that underpin changes in local population structure in the presence of a key mutualistic partner.
Project description:Cleaning behaviour is deemed a mutualism, however the benefit of cleaning interactions to client individuals is unknown. Furthermore, mechanisms that may shift fish community structure in the presence of cleaning organisms are unclear. Here we show that on patch reefs (61-285 m²) which had all cleaner wrasse Labroides dimidiatus (Labridae) experimentally removed (1-5 adults reef?¹) and which were then maintained cleaner-fish free over 8.5 years, individuals of two site-attached (resident) client damselfishes (Pomacentridae) were smaller compared to those on control reefs. Furthermore, resident fishes were 37% less abundant and 23% less species rich per reef, compared to control reefs. Such changes in site-attached fish may reflect lower fish growth rates and/or survivorship. Additionally, juveniles of visitors (fish likely to move between reefs) were 65% less abundant on removal reefs suggesting cleaners may also affect recruitment. This may, in part, explain the 23% lower abundance and 33% lower species richness of visitor fishes, and 66% lower abundance of visitor herbivores (Acanthuridae) on removal reefs that we also observed. This is the first study to demonstrate a benefit of cleaning behaviour to client individuals, in the form of increased size, and to elucidate potential mechanisms leading to community-wide effects on the fish population. Many of the fish groups affected may also indirectly affect other reef organisms, thus further impacting the reef community. The large-scale effect of the presence of the relatively small and uncommon fish, Labroides dimidiadus, on other fishes is unparalleled on coral reefs.
Project description:Humans and other animals use previous experiences to make behavioural decisions, balancing the probabilities of receiving rewards or punishments with alternative actions. The dopaminergic system plays a key role in this assessment: for instance, a decrease in dopamine transmission, which is signalled by the failure of an expected reward, may elicit a distinct behavioural response. Here, we tested the effect of exogenously administered dopaminergic compounds on a cooperative vertebrate's decision-making process, in a natural setting. We show, in the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus, that blocking dopamine receptors in the wild induces cleaners to initiate more interactions with and to provide greater amounts of physical contact to their client fish partners. This costly form of tactile stimulation using their fins is typically used to prolong interactions and to reconcile with clients after cheating. Interestingly, client jolt rate, a correlate of cheating by cleaners, remained unaffected. Thus, in low effective dopaminergic transmission conditions cleaners may renegotiate the occurrence and duration of the interaction with a costly offer. Our results provide first evidence for a prominent role of the dopaminergic system in decision-making in the context of cooperation in fish.
Project description:Testing performance in controlled laboratory experiments is a powerful tool for understanding the extent and evolution of cognitive abilities in non-human animals. However, cognitive testing is prone to a number of potential biases, which, if unnoticed or unaccounted for, may affect the conclusions drawn. We examined whether slight modifications to the experimental procedure and apparatus used in a spatial task and reversal learning task affected performance outcomes in the bluestreak cleaner wrasse, Labroides dimidiatus (hereafter "cleaners"). Using two-alternative forced-choice tests, fish had to learn to associate a food reward with a side (left or right) in their holding aquarium. Individuals were tested in one of four experimental treatments that differed slightly in procedure and/or physical set-up. Cleaners from all four treatment groups were equally able to solve the initial spatial task. However, groups differed in their ability to solve the reversal learning task: no individuals solved the reversal task when tested in small tanks with a transparent partition separating the two options, whereas over 50% of individuals solved the task when performed in a larger tank, or with an opaque partition. These results clearly show that seemingly insignificant details to the experimental set-up matter when testing performance in a spatial task and might significantly influence the outcome of experiments. These results echo previous calls for researchers to exercise caution when designing methodologies for cognition tasks to avoid misinterpretations.