Date Published: July 6, 2017
Publisher: Public Library of Science
Author(s): Marta C. Soares, Sónia C. Cardoso, Renata Mazzei, Gonçalo I. André, Marta Morais, Magdalena Gozdowska, Hanna Kalamarz-Kubiak, Ewa Kulczykowska, Sylvie Rétaux.
Social relationships are crucially dependent on individual ability to learn and remember ecologically relevant cues. However, the way animals recognize cues before engaging in any social interaction and how their response is regulated by brain neuromodulators remains unclear. We examined the putative involvement of arginine vasotocin (AVT) and isotocin (IT), acting at different brain regions, during fish decision-making in the context of cooperation, by trying to identify how fish distinguish and recognize the value of other social partners or species. We hypothesized that the behavioural responses of cleaner fish clients to different social contexts would be underlain by changes in brain AVT and IT levels. We have found that changes in AVT at the level of forebrain and optic tectum are linked with a response to allopatric cleaners (novel or unfamiliar stimuli) while those at cerebellum are associated with the willingness to be cleaned (in response to sympatric cleaners). On the other hand, higher brain IT levels that were solely found in the diencephalon, also in response to allopatric cleaners. Our results are the first to implicate these nonapeptides, AVT in particular, in the assessment of social cues which enable fish to engage in mutualistic activities.
Social relationships are crucially dependent on individual ability to learn and remember beneficial cues . The ability to pay attention to specific key information linked to other individuals or species is a prerequisite for animals that live in complex social systems. For instance, cues indicating that an animal is being watched, i.e., has an audience, lead to increases in levels of cooperation [2,3]. Social discrimination acquires a new dimension when occurring in cooperative or mutualistic contexts, as individuals’ decisions will determine the amount of benefits they gain but also depend on the responses of other individuals [4–6]. Typically, the term cooperation refers to a relationship between relatives in which both may asymmetrically benefit from the association [7,8], while the term mutualism is more specific to a similar cooperative relationship but this time, occurring between two different species .
In nature, individuals must navigate complex social environments. Here, we introduced clients to treatments that differed substantially: a) the conspecific context was both familiar and social, b) the sympatric cleaner condition was familiar, cooperative, and social, c) the allopatric cleaner condition was novel, social, and potentially unsafe and d) the control condition was non-social and novel. Specifically, we showed that clients i) engaged mostly in agonistic interactions with conspecifics, primarily on cleaning interactions with sympatric cleaners, ii) did not engage in agonist or cleaning interactions with allopatric cleaners and iii) were similarly interactively absent in the control context (see Fig 1 for experimental setup); we found that both nonapeptide levels (AVT and IT) differed overall across some specific brain regions, changing in accordance to specific treatment. We found that clients in contact with allopatric cleaners had higher levels of AVT in the forebrain and the optic tectum than those introduced to sympatric cleaners. On the other hand, clients in contact with sympatric cleaners showed lower levels of AVT in the cerebellum compared to those kept with a ball. Moreover, levels of IT were higher in subjects in contact with allopatric cleaners when compared to sympatric cleaners and conspecifics only at the diencephalon. Our results are the first to link these nonapeptides with the variation of client social behaviour and probability to engage in cooperative interactions in fish.