João P. M. Messias

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.

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.

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.

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.

Correction to: Stimulation of dopamine D1 receptor improves learning capacity in cooperating cleaner fish

[ Proc. R. Soc. B 283 , 20152272. (20 January 2016; Published online 20 January 2016) ([doi:10.1098/rspb.2015.2272][2])][2] We recently discovered an error in the article cited above: we realized that the order of treatments did not seem to be counterbalanced in the cue discrimination task during

Erratum to: When good advertisement backfires: cleaners get eaten too

Soares MC, Bshary R, Cardoso SC, Cote IM, Oliveira RF (2012) Face Your fears: cleaning Gobies inspect predators despite being stressed by them. PLoS ONE 7(6):e39781. doi:10.1371/journal. pone.0039781 Soares MC, Cardoso SC, Grutter AS, Oliveira RF, Bshary R (2014) Cortisol mediates cleaner wrasse switch from cooperation to cheating and tactical deception. Horm Behav 66:346–350 Paula JR, Messias JPM, Grutter AS, Bshary R, Soares MC (2015) The role of serotonin in the modulation of cooperative behavior. Behav Ecol. doi:10.1093/beheco/arv039