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

João P M Messias,Svante Winberg,Murilo S Abreu,Marta C Soares,Per-Ove Thörnqvist

doi:10.1038/s41598-018-25513-6

João P M Messias, Svante Winberg + Show 3 more

Open Access

https://doi.org/10.1038/s41598-018-25513-6

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Abstract

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.

Highlights

The monoamines, serotonin (5-HT) and dopamine (DA), are essential neurotransmitters in the central nervous system
Monoamines are crucially involved in the orchestration of behaviour in vertebrates and invertebrates[14,15,16,17], from simple to more complex social outputs that require coordination between two or more individuals18,19. 5-HT is best known to be responsible for the regulation of social motivation or mood in vertebrates, including humans[20,21,22], variation in levels may be associated with antisocial behaviours and aggressive responses[23,24]
The frequency of cleaning interactions was significantly higher when clients were exposed to a cleaner compared to those exposed to another conspecific, and the same occurred with the mean interaction time, the frequency of cleaning bites, the proportion of interactions with tactile stimulation and the proportion of time providing tactile stimulation, except for the incidence of chases which showed the opposite trend (Table 1)

Summary

Introduction

The monoamines, serotonin (5-HT) and dopamine (DA), are essential neurotransmitters in the central nervous system. The vertebrate dopaminergic system is comprised of projections that originate in the posterior tubercular orthopedia-dependent neurons, which include the individual somata integrating the ascending DA system, the descending diencephalospinal, as well as the endohypothalamic, circuitry[5] These monoamines (5-HT and DA) are found in practically all brain regions[6,7], and in individuals from all major species’ groups (e.g., mollusks[8,9], teleost fish[10,11] and humans[12,13]). One the best-known species of cleaner fish is the Indo-Pacific cleaner wrasse, Labroides dimidiatus, which undertakes interspecific cooperative interactions as means to secure energy In this system, simple foraging has been replaced by a series of cognitive sophisticated behaviours that include: individual recognition of clients, manipulation of client decisions (on distinct levels of action), reconciliation, punishment, advertising of their cleaning services, tactical deception and indirect reciprocity based on image scoring (reviewed by[43]). The modulation of learning in the context of interspecific sociality seems to be strongly associated with the increase in signaling of the dopamine D1 receptor[47,48], and the attribution of motivational salience to cue-signals[49]

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