Sónia C. Cardoso

Client preferences by Caribbean cleaning gobies: food, safety or something else?

Predation risk is amongst the most pervasive selective pressures influencing behaviour and animals have been repeatedly shown to trade-off foraging success for safety. We examined the nature of this trade-off in cleaning symbioses amongst Caribbean coral reef fishes. We predicted that cleaning gobies (Elacatinus evelynae and Elacatinus prochilos) should prefer fish clients that pose a low risk of predation (e.g. herbivores) over clients that may have more ectoparasites but pose a higher risk (e.g. piscivores). Our field observations revealed that cleaners did clean preferentially client species with more parasites but predatory and non-predatory clients had similar ectoparasite loads. Despite the lack of a foraging advantage for inspecting predators, cleaners did not avoid risky clients. On the contrary, a larger proportion of visiting predators than non-predators was inspected, gobies initiated more interactions with predatory clients, and predators were attended to immediately upon arrival at cleaning stations. This preferential treatment of dangerous clients may allow the rapid identification of cleaners as non-prey item or may be due to the effect of predators on the rest of the cleaners’ clientele, which avoided cleaning stations whilst predators were present. Dealing with potentially risky clients may allow gobies to regain access to their main food source: non-predatory clients.

Face your fears: cleaning gobies inspect predators despite being stressed by them.

Social stressors typically elicit two distinct behavioural responses in vertebrates: an active response (i.e., “fight or flight”) or behavioural inhibition (i.e., freezing). Here, we report an interesting exception to this dichotomy in a Caribbean cleaner fish, which interacts with a wide variety of reef fish clients, including predatory species. Cleaning gobies appraise predatory clients as potential threat and become stressed in their presence, as evidenced by their higher cortisol levels when exposed to predatory rather than to non-predatory clients. Nevertheless, cleaning gobies neither flee nor freeze in response to dangerous clients but instead approach predators faster (both in captivity and in the wild), and interact longer with these clients than with non-predatory clients (in the wild). We hypothesise that cleaners interrupt the potentially harmful physiological consequences elicited by predatory clients by becoming increasingly proactive and by reducing the time elapsed between client approach and the start of the interaction process. The activation of a stress response may therefore also be responsible for the longer cleaning service provided by these cleaners to predatory clients in the wild. Future experimental studies may reveal similar patterns in other social vertebrate species when, for instance, individuals approach an opponent for reconciliation after a conflict.

Interspecific differences in foraging behaviour and functional role of Caribbean parrotfish

Herbivory is one of the most important biological processes influencing coral reefs. In the highly diverse Indo-Pacific reef fish communities, different herbivores can have strikingly different functions. We investigated the extent of functional diversity among herbivorous parrotfish of the more species-depauperate Caribbean Sea. We carried out observations of seven species of parrotfish (Scarus taeniopterus, Sc. vetula, Sc. iserti, Sparisoma viride, Sp. aurofrenatum, Sp. rubripinne and Sp. chrysopterum) on four Barbadian coral reefs to collect information on foraging techniques, rates, and targets, and found marked interspecific variation. Species of the genus Scarus had higher foraging rates than those of the genus Sparisoma . Different species took varying amounts of live coral, turf algae and macroalgae. A functional categorization based first on foraging technique (contact or no contact with the substratum) and secondarily on the more conventional criterion of foraging target (macroalgae, turf algae and live coral) allowed us to classify Sc. taeniopterus and Sc. iserti as ‘scrapers’, Sp. aurofrenatum , Sp. rubripinne and Sp. chrysopterum as ‘grazers’, Sp. viride as a ‘bioeroder’ and Sc. vetula as a ‘bioeroder/scraper’. This functional group affiliation, together with species-specific foraging rates, allows us to predict the role of Caribbean parrotfish on major coral reef processes and their impact on coral reef benthic communities.

Arginine vasotocin modulates associative learning in a mutualistic cleaner fish

Social environmental complexity induces structural and biochemical changes in animals’ brains, which are linked to the improvement of animals’ learning abilities. The nonapeptides from the arginine vasopressin (AVP) family (arginine vasotocin, AVT, in non-mammals) play a significant role in the regulation of social behavior, particularly in the formation of social memories and individual recognition. Moreover, the role of AVT in the regulation of interspecific interactions has only recently started to be addressed in the context of cleaner fish mutualisms and learning. Variance in the distribution of AVP receptor expression, which is linked to distinct neural systems (related to the dorsolateral and the dorsomedial telencephalon), is known to be implicated in differences in individual learning processes. Here we asked if the associative learning performance of the Indo-Pacific bluestreak cleaner wrasse (Labroides dimidiatus) is regulated by AVT. We tested the influence of AVT upon the cleaners’ ability to solve two different problems (cue and place discrimination tasks) that in principle differ in ecological relevance and are associated with two different memory systems. We found that AVT affected the learning competence of cleaners differently between tasks, as individual performance showed distinct response selectivity to AVT dosage levels. However, only in the ecologically relevant task was their learning response improved by blocking AVT via treatment with the antagonist Manning compound. Our findings demonstrate that AVT pathways, which are implicated in the regulation of interspecific behavior (i.e., a cleaner’s willingness to seek interactions with clients), are also linked to individual learning ability in the context of mutualistic behavior, and in tune with socio-ecological demands.

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.

Indo-Pacific parrotfish exert partner choice in interactions with cleanerfish but Caribbean parrotfish do not

Cooperation theory puts a strong emphasis on partner control mechanisms that have evolved to stabilize cooperation against the temptation of cheating. The marine cleaning mutualism between the IndoPacific bluestreack cleaner wrasse, Labroides dimidiatus, and its reef fish ‘clients’ has been a model system to study partner control mechanisms and counterstrategies. These cleaners cooperate by eating ectoparasites; however, they can cheat by taking client mucus, which they prefer. Such a conflict may be the exception. For example, Caribbean cleaning gobies, Elacatinus spp., prefer to eat ectoparasites instead of mucus. While partner control mechanisms and counterstrategies seem to be absent in cleaning gobies, no study has directly compared cleaner wrasses and cleaning gobies by using the same methods. We examined systematic differences in cleaning interaction patterns and strategic behaviour exhibited by 12 closely related parrotfish species in the two systems. Parrotfish seeking cleaner wrasses visited them more often and spent more time with their cleaner than parrotfish seeking cleaning gobies. Moreover, the clients of cleaner wrasses returned more often to the same cleaner following a positive interaction, whereas the clients of cleaning gobies were less influenced by the outcome of previous interactions. We hypothesize that the higher frequency and repeated nature of interactions observed in the cleaner wrasse system, combined with the need to resolve conflicts, might have been prerequisites for the development of complex behavioural strategies.

Region specific changes in nonapeptide levels during client fish interactions with allopatric and sympatric cleaner fish

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.

Using model fish to study the biological mechanisms of cooperative behaviour: A future for translational research concerning social anxiety disorders?

Human societies demand of its composing members the development of a wide array of social tools and strategies. A notable example is human outstanding ability to cooperate with others, in all its complex forms, depicting the reality of a highly demanding social framework in which humans need to be integrated as to attain physical and mental benefits. Considering the importance of social engagement, its not entirely unexpected that most psychiatric disorders involve some disruption of normal social behaviour, ranging from an abnormal absence to a significant increase of social functioning. It is however surprising that knowledge on these social anxiety disorders still remains so limited. Here we review the literature focusing on the social and cooperative toolbox of 3 fish model species (cleaner fishes, guppies and zebrafish) which are amenable systems to test for social disorders. We build on current knowledge based on ethological information, arising from studies on cooperative behaviour in cleanerfishes and guppies, while profiting from the advantages of the intense use of zebrafish, to create novel paradigms aiming at the major socio-cognitive modules/dimensions in fish species. This focus may enable the discovery of putative conserved endpoints which are relevant for research into social disorders. We suggest that cross-species, cross-domain, functional and genetic approaches could provide a wider array of information on the neurobiological bases of social and cooperative behaviour, crucial to understanding the neural bases of social disorders and key to finding novel avenues towards treatment.

Profiles of cooperative brains: A discriminant analysis of cleaner and client fish monoaminergic responses to different social contexts

Vertebrate cognitive function requires a dynamic coordination of multiple specialized areas of the brain. The challenge here is to understand how these brain areas respond in dependence to the neurophysiological mechanisms in place, as to enable the successful processing of information. For instance, social and cooperative behaviour has been linked to the activation of some specific brain areas, mostly associated with reward processing, however mechanisms could in principle change, in accordance to species social demands and taxon involved. Here we chose a classic model system of cooperation between species of fish and compared the brain monoaminergic response of cleaners Labroides dimidiatus exposed to several social-related treatments to the response of one client species (Naso elegans) introduced to similar contexts. We demonstrate that the variable appraisal of each social challenge contributes to brain dopaminergic and serotonergic changes, in cleaners and clients, with both showing the diencephalon and optic tectum as main areas of metabolite response. However, the role of the serotoninergic system activation was mostly demonstrated at the diencephalon and cerebellum of cleaners, a response that was driven by the exposure to clients. Our current results are the first to jointly demonstrate the level of selective similarity in brain monoaminergic mechanisms that underlie fish mutualistic and social engagement, for both sides of these partnerships.