Browsing by Author "Bshary, Redouan"
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- Arginine vasotocin modulates associative learning in a mutualistic cleaner fishPublication . Cardoso, Sónia C.; Bshary, Redouan; Mazzei, Renata; Paitio, José R.; Oliveira, Rui Filipe; Soares, Marta C.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.
- Arginine vasotocin reduces levels of cooperative behaviour in a cleaner fishPublication . Cardoso, Sónia C.; Paitio, José R.; Oliveira, Rui Filipe; Bshary, Redouan; Soares, Marta C.Cooperation between unrelated individuals usually involves investments that often mean a decrease in immediate payoffs, but ensure future benefits. Here we investigated the potential role of the neuropeptides Arginine-vasotocin (AVT) and Isotocin (IT) as proximate agents affecting individuals' cooperative levels in the Indo-pacific bluestreak cleanerwrasse Labroides dimidiatus. Their ‘client’ reef fish partners only benefit from interacting if cleaners eat ectoparasites and refrain from gleaning preferred clientmucus. Thus, cleaners must control their impulse to eat according to their preference, and eat less preferred items to maintain ongoing interactions and avoid clients' leaving or punishing. We found that solely the experimental transient higher dosage of AVT led to a decrease of cleaners'willingness to feed against their preference, while IT and AVT antagonists had no significant effects. The sole effect of AVT on cleaner's performance may imply a link between AVT's influence and a potential activation of a stress response. Our results confirm the importance of the AVT/AVP system as an agent affecting levels of cooperation, offering a potential mechanistic pathway for the reported flexible service quality that cleaners provide their clients.
- Arginine vasotocin regulation of interspecific cooperative behaviour in a cleaner fishPublication . Soares, Marta C.; Bshary, Redouan; Mendonça, Rute; Grutter, Alexandra S.; Oliveira, Rui FilipeIn an interspecific cooperative context, individuals must be prepared to tolerate close interactive proximity to other species but also need to be able to respond to relevant social stimuli in the most appropriate manner. The neuropeptides vasopressin and oxytocin and their non-mammalian homologues have been implicated in the evolution of sociality and in the regulation of social behaviour across vertebrates. However, little is known about the underlying physiological mechanisms of interspecific cooperative interactions. In interspecific cleaning mutualisms, interactions functionally resemble most intraspecific social interactions. Here we provide the first empirical evidence that arginine vasotocin (AVT), a non-mammalian homologue of arginine vasopressin (AVP), plays a critical role as moderator of interspecific behaviour in the best studied and ubiquitous marine cleaning mutualism involving the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus. Exogenous administration of AVT caused a substantial decrease of most interspecific cleaning activities, without similarly affecting the expression of conspecific directed behaviour, which suggests a differential effect of AVT on cleaning behaviour and not a general effect on social behaviour. Furthermore, the AVP-V1a receptor antagonist (manning compound) induced a higher likelihood for cleaners to engage in cleaning interactions and also to increase their levels of dishonesty towards clients. The present findings extend the knowledge of neuropeptide effects on social interactions beyond the study of their influence on conspecific social behaviour. Our evidence demonstrates that AVT pathways might play a pivotal role in the regulation of interspecific cooperative behaviour and conspecific social behaviour among stabilized pairs of cleaner fish. Moreover, our results suggest that the role of AVT as a neurochemical regulator of social behaviour may have been co-opted in the evolution of cooperative behaviour in an interspecific context, a hypothesis that is amenable to further testing on the potential direct central mechanism involved.
- Brain morphology predicts social intelligence in wild cleaner fishPublication . Triki, Zegni; Emery, Yasmin; Teles, Magda C; Oliveira, Rui Filipe; Bshary, RedouanIt is generally agreed that variation in social and/or environmental complexity yields variation in selective pressures on brain anatomy, where more complex brains should yield increased intelligence. While these insights are based on many evolutionary studies, it remains unclear how ecology impacts brain plasticity and subsequently cognitive performance within a species. Here, we show that in wild cleaner fish (Labroides dimidiatus), forebrain size of high-performing individuals tested in an ephemeral reward task covaried positively with cleaner density, while cerebellum size covaried negatively with cleaner density. This unexpected relationship may be explained if we consider that performance in this task reflects the decision rules that individuals use in nature rather than learning abilities: cleaners with relatively larger forebrains used decision-rules that appeared to be locally optimal. Thus, social competence seems to be a suitable proxy of intelligence to understand individual differences under natural conditions.
- Caribbean cleaning gobies prefer client ectoparasites over mucusPublication . Soares, Marta C.; Côté, Isabelle M.; Cardoso, Sónia C.; Oliveira, Rui Filipe; Bshary, RedouanIf cooperation often involves investment, then what specific conditions prevent selection from acting on cheaters that do not invest? The mutualism between the Indo-Pacific cleaner wrasse Labroides dimidiatus and its reef fish clients has been a model system to study conflicts of interest and their resolution. These cleaners prefer client mucus over ectoparasites – that is, they prefer to cheat – but punishment and partner switching by clients enforce cooperative behaviour by cleaners. By contrast, clients of Caribbean cleaning gobies (Elacatinus spp.) do not to use punishment or partner switching. Here, we test the hypothesis that the behavioural differences between these two cleaner fish systems are caused by differences in cleaner foraging preferences. In foraging choice experiments, we offered broadstripe cleaning gobies Elacatinus prochilos client-derived parasitic isopods, client mucus and a control food item. The cleaning gobies significantly preferred ectoparasites over mucus or the control item, which contrasts with cleaner wrasses. We propose that the low level of cleaner–client conflict arising from cleaning goby foraging preferences explains the observed lack of strategic partner control behaviour in the clients of cleaning gobies.
- Cleaning in pairs enhances honesty in male cleaning gobiesPublication . Soares, Marta C.; Bshary, Redouan; Côté, Isabelle M.A recent game theoretic model akin to an iterated prisoner’s dilemma explored situations in which 2 individuals (the service providers) interact simultaneously with the same service recipient (the client). If providing a dishonest service pays, then each service provider may be tempted to cheat before its partner, even if cheating causes the client’s departure; however, a theoretical cooperative solution also exists where both partners should reduce cheating rates. This prediction is supported by indirect measures of cheating (i.e., inferred from client responses) by pairs of Indo-Pacific bluestreak cleaner wrasses Labroides dimidiatus. Here, we examine how inspecting in pairs affects service quality in Caribbean cleaning gobies Elacatinus spp. We measured dishonesty directly by examining the stomach contents of solitary and paired individuals and calculating the ratio of scales to ectoparasites ingested. We found that the propensity to cheat of females and males differed: females always cleaned relatively honestly, whereas males cheated less when cleaning in pairs than when cleaning alone. However, overall, the cleaning service of single and paired individuals was similar. Our results confirm that cleaners cooperate when cleaning in pairs; however, our findings differ from the specific predictions of the model and the observations on L. dimidiatus. The differences may be due to differences in mating systems and cleaner–client interactions between the 2 cleaner fish species
- Cortisol mediates cleaner wrasse switch from cooperation to cheating and tactical deceptionPublication . Soares, Marta C.; Cardoso, Sónia C.; Grutter, Alexandra S.; Oliveira, Rui Filipe; Bshary, RedouanRecent empirical research, mostly done on humans, recognizes that individuals' physiological state affects levels of cooperation. An individual's internal state may affect the payoffs of behavioural alternatives, which in turn could influence the decision to either cooperate or to defect. However, little is known about the physiology underlying condition dependent cooperation. Here, we demonstrate that shifts in cortisol levels affect levels of cooperation in wild cleaner wrasse Labroides dimidiatus. These cleaners cooperate by removing ectoparasites from visiting ‘client’ reef fishes but prefer to eat client mucus, which constitutes cheating. We exogenously administrated one of three different compounds to adults, that is, (a) cortisol, (b) glucocorticoid receptor antagonist mifepristone RU486 or (c) sham(saline), and observed their cleaning behaviour during the following 45 min. The effects of cortisol match an earlier observational study that first described the existence of “cheating” cleaners: such cleaners provide small clients with more tactile stimulation with their pectoral and pelvic fins, a behaviour that attracts larger clients that are then bitten to obtain mucus. Blocking glucocorticoid receptors led to more tactile stimulation to large clients. As energy demands and associated cortisol concentration level shifts affect cleaner wrasse behavioural patterns, cortisol potentially offers a general mechanism for condition dependent cooperation in vertebrates.
- Do cleaning organisms reduce the stress response of client reef fish?Publication . Bshary, Redouan; Oliveira, Rui Filipe; Oliveira, Tânia Sofia Ferreira de; Canário, Adelino V. M.Background: Marine cleaning interactions in which cleaner fish or shrimps remove parasites from visiting 'client' reef fish are a textbook example of mutualism. However, there is yet no conclusive evidence that cleaning organisms significantly improve the health of their clients. We tested the stress response of wild caught individuals of two client species, Chromis dimidiata and Pseudanthias squamipinnis, that had either access to a cleaner wrasse Labroides dimidiatus, or to cleaner shrimps Stenopus hispidus and Periclimenes longicarpus, or no access to cleaning organisms. Results: For both client species, we found an association between the presence of cleaner organisms and a reduction in the short term stress response of client fish to capture, transport and one hour confinement in small aquaria, as measured with cortisol levels. Conclusion: It is conceivable that individuals who are more easily stressed than others pay a fitness cost in the long run. Thus, our data suggest that marine cleaning mutualisms are indeed mutualistic. More generally, measures of stress responses or basal levels may provide a useful tool to assess the impact of interspecific interactions on the partner species.
- Does access to the bluestreak cleaner wrasse Labroides dimidiatus affect indicators of stress and health in resident reef fishes in the Red Sea?Publication . Ros, Albert F. H.; Lusa, Jeanne; Meyer, Meghann; Soares, Marta C.; Oliveira, Rui Filipe; Brossard, Michel; Bshary, RedouanInteractions between the bluestreak cleaner wrasse Labroides dimidiatus and its client reef fish are a textbook example of interspecific mutualism. The fact that clients actively visit cleaners and invite inspection, together with evidence that cleaners eat many client ectoparasites per day, indeed strongly suggests a mutualistic relationship. What remains unknown is how parasite removal affects the physiology of clients and thereby their body condition, health, and immune function. Here we addressed these issues in a field study in Ras Mohammed National Park, Egypt. In our study area, small reef patches are inter-spaced with areas of sandy substrate, thereby preventing many species (i.e., residents, including cleaner wrasses) from travelling between the reef patches. This habitat structure leads to a mosaic of resident clients with and without access to bluestreak cleaner wrasses, further referred to as “cleaner access”, on which we focused our study. We found that residents with cleaner access had higher body condition than residents without cleaner access. However, indicators of stress like variation in cortisol levels corrected for handling time and various immune parameters were apparently unaffected by cleaner access. In fact antibody responses were significantly higher in fishes without cleaner access. This suggests that cleaner access decreases the need for active immunity and that this releases resources that might be allocated to other functions such as somatic growth and reproduction.
- Expanding the concept of social behavior to interspecific interactionsPublication . Oliveira, Rui F.; Bshary, RedouanIn pretty much any species, an individual's survival and reproduction depends crucially on the outcome of interactions with other individuals. Key interactions may take place between individuals of the same species but also between individuals belonging to different species. However, the most accepted definition of social behavior only considers interactions between conspecifics. Here, we argue that the distinction between intra- and interspecific interactions is largely artificial and hinders the integration of the historically separately developed concepts. At the ultimate level, given that the ecological landscape of organisms is composed both by interactions with conspecifics and with heterospecifics, and both types of interactions may have evolutionary consequences. Although intraspecific interactions usually have a higher impact in fitness because in most species interactions relevant for reproduction (mating, parenting) exclusively involve conspecifics, and interactions relevant for survival are more probable between conspecifics because they share the same ecological niche, hence competing for the same resources (e.g., food, shelter), there are notable exceptions in both fitness components (e.g., heterospecific mating in parthenogenic all-female species; heterospecific brood parasitism; heterospecific aggression in sympatric species that compete for shared resources). At the proximate level, behaviors and cognitive decision-making rules used to interact with other organisms may be shared between intra- and interspecific interactions, and the mechanistic differences between conspecific social behaviors used in distinct functional domains, such as mating, aggression, or parenting, can be more expressive than those found within the same functional domain between conspecific and heterospecific behavior. Therefore, there are neither fundamental conceptual (ultimate) reasons, nor key differences in mechanisms underlying behaviors involved in conspecific vs. heterospecific interactions that support the exclusion of interspecific interactions from the conceptual framework of social behavior