The variable monoaminergic outcomes of cleaner fish brains when facing different social and mutualistic contexts.

The monoamines serotonin and dopamine are important neuromodulators present in the central nervous system, known to be active regulators of social behaviour in fish as in other vertebrates. Our aim was to investigate the region-specific brain monoaminergic differences arising when individual cleaners face a client (mutualistic context) compared to when they are introduced to another conspecific (conspecific context), and to understand the relevance of visual assessment compared to the impact of physical contact with any partner. We demonstrated that serotoninergic activity at the diencephalon responds mostly to the absence of physical contact with clients whereas cerebellar dopaminergic activity responds to actual cleaning engagement. We provide first insights on the brain's monoaminergic (region-specific) response variations, involved in the expression of cleaner fishes' mutualistic and conspecific behaviour. These results contribute to a better understanding of the monoaminergic activity in accordance to different socio-behavioural contexts.

Monoaminergic levels at the forebrain and diencephalon signal for the occurrence of mutualistic and conspecific engagement in client reef fish.

Social interactions are commonly found among fish as in mammals and birds. While most animals interact socially with conspecifics some however are also frequently and repeatedly observed to interact with other species (i.e. mutualistic interactions). This is the case of the (so-called) fish clients that seek to be cleaned by other fish (the cleaners). Clients face an interesting challenge: they raise enough motivation to suspend their daily activities as to selectively visit and engage in interactions with cleaners. Here we aimed, for the first time, to investigate the region-specific brain monoaminergic level differences arising from individual client fish when facing a cleaner (interspecific context) compared to those introduced to another conspecific (socio-conspecific context). We show that monoaminergic activity differences occurring at two main brain regions, the diencephalon and the forebrain, are associated with fish clients' social and mutualistic activities. Our results are the first demonstration that monoaminergic mechanisms underlie client fish mutualistic engagement with cleanerfish. These pathways should function as a pre-requisite for cleaning to occur, providing to clients the cognitive and physiological tools to seek to be cleaned.

Estradiol shapes mutualistic behaviour of female cleaner fish (Labroides dimidiatus - Valenciennes, 1839): Potential implications of environmental disturbance.

The presence of endocrine-derived compounds in the environment occurs due to a myriad of human or industrial activity and can disrupt the endocrine system of animals, including fish. One important group of endocrine disruptors are the estrogens, such as 17-ß estradiol (E2, estradiol). Estrogens are gonadal steroid hormones, able to be influential even in small concentrations. Here, we demonstrate that E2 is linked to female' decisions made by an important coral reef species, the cleaner fish Labroides dimidiatus, during interactions with other reef fishes (known as clients). E2 treatment in natural conditions interfered directly in the cooperative relationships, by increasing cleaners' willingness to interact with clients, providing greater amounts of physical contact to their fish partners. We discuss the meaning of the observed behavioural disruption produced by E2, which by affecting a key species (cleaners) may produce a cascade impact in the aquatic ecosystem.

Dopamine disruption increases cleanerfish cooperative investment in novel client partners.

Social familiarization is a process of gaining knowledge that results from direct or indirect participation in social events. Cooperative exchanges are thought to be conditional upon familiarity with others. Indeed, individuals seem to prefer to engage with those that have previously interacted with them, which are more accurate predictors of reward than novel partners. On the other hand, highly social animals do seek novelty. Truth is that the physiological bases underlying how familiarity and novelty may affect cooperative decision-making are still rather obscure. Here, we provide the first experimental evidence that the level of the dopaminergic influence in cooperative exchanges is constrained to mechanisms of social familiarization and novelty in a cleanerfish, Labroides dimidiatus. Cleaners were tested against familiar and novel Ctenochaetus striatus surgeonfish (a common client species) in laboratorial conditions, and were found to spend more time providing physical contact (also referred to as tactile stimulation) to familiar fish clients. Cleaners use tactile stimulation as a way to reduce the risk of a non-rewarding outcome, a behavioural response that is even more pronounced when blocking dopamine (DA) D1 receptors. We discovered that the influence of DA disruption on cleaners' provision of physical contact was dependent on the level of familiarity with its partner, being highly exacerbated whenever the client is novel, and unnoticed when dealing with a familiar one. Our findings demonstrate that DA mediation influences the valuation of partner stimuli and the enhancing investment in novel partners, mechanisms that are similar to other vertebrates, including humans.

Can cleanerfish overcome temptation? A selective role for dopamine influence on cooperative-based decision making.

Evidence suggests that animals are selected to make accurate choices and prioritize goals within the constraints of a given social environment to maximize fitness. These decisions are mostly based on complex processes in which value is linked to reward and cues may carry variable incentive salience. However, the level in which the incentive elicited by a cue is able to shift individual choices should differ between individuals and neurophysiological states. Here we used a notorious cooperative cleanerfish species Labroides dimidiatus to probe for differences in the incentive motivational valences given to food cues and then tested for the role of the dopaminergic system in the appraisal of such cues. We found that cleaners differed in Pavlovian conditioned approach behavioural responses to reward-associated stimuli: while the majority were fast to engage physically with the cue plate that indicated future reward delivery (sign trackers), only a few took significantly more time to respond (goal trackers). But amongst those that were considering the sole cue attractive, we discovered that the dopaminergic blockage decreased their initial propensity to approach and touch the cue plate. Our results show that dopamine disruption contributes to shifting the attribution of motivational incentive from the predictive cue towards the actual reward and provides key insight into the physiological framework of cooperative-based decision making.

Dopamine disruption increases negotiation for cooperative interactions in a fish.

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.

Stimulation of dopamine D1 receptor improves learning capacity in cooperating cleaner fish.

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.