Redouan Bshary

Université de Neuchâtel, Neuenburg, Neuchâtel, Switzerland

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Publications (137)750.22 Total impact

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    Redouan Bshary · Rui F Oliveira
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    ABSTRACT: Standard approaches to study the evolution and stability of helping either investigate how life history features like longevity and migration may yield conditions that select for rather unconditional helping or how specific game structures yield conditional helping strategies. Although the latter approach is more apt at explaining variable behavior within and between individuals, applicability seems limited due to strong compartmentalization of situations. Instead, recent evidence suggests that individuals are primarily under selection to display general social competence, that is, the ability to choose among the full range of available social behaviors the one that is appropriate to maximize fitness within the constraints of given circumstances. This view shifts the emphasis to general decision rules and the evolution of developmental mechanisms.
    06/2015; 3:31-37. DOI:10.1016/j.cobeha.2015.01.008
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    ABSTRACT: 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.
    Behavioral Ecology and Sociobiology 05/2015; DOI:10.1007/s00265-015-1931-z · 3.05 Impact Factor
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    ABSTRACT: In mammals it has been proposed that complex social environments have selected for sophisticated social strategies. Third-party and more specifically third-party rank relationship knowledge is an important requirement for such strategies, especially in species with a strict hierarchy such as primates. Previous research has demonstrated that female vervet monkeys know the entire female hierarchy within their group, suggesting a detailed knowledge of their surrounding social world. What remains unclear, however, is the extent and detail of such social knowledge in other age/sex classes. We used the same experimental design to test whether females and males also keep track of each other's hierarchy and whether juveniles know about the female hierarchy. Our results suggest that females know about the male hierarchy but that males and juveniles seem to lack such knowledge regarding the female hierarchy. This indicates sex and developmental differences in the extent of social knowledge and especially third-party rank relationship knowledge in vervet monkeys. As a consequence, sophisticated social strategies may most likely be found in adult females in this species.
    Animal Behaviour 04/2015; 102. DOI:10.1016/j.anbehav.2015.02.006 · 3.14 Impact Factor
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    ABSTRACT: Studies on different vertebrate groups have provided evidence that androgen levels in males increase after competitive social interactions during the breeding season, as postulated by the Challenge Hypothesis. However, social modulation of androgen levels may vary with latitude and may differ between species holding seasonal versus year-round territories. Here, we tested the Challenge Hypothesis on a seasonal tropical damselfish, Abudefduf sexfasciatus, where males temporarily defend territory and eggs against both intra- and interspecific individuals. Carrying out simulated territorial intrusions (STIs) in the laboratory, we document for the first time a consistent increase in the plasma level of the androgen precursor 11-ketoandrostenedione (11KA) in fish confronted to either intra- or interspecific challenges. Collecting samples in the field also revealed higher 11KA levels in fish facing frequent territorial interactions than in non-territorial individuals. Levels of 11-ketotestosterone (11KT) were high in territorial males in the field, but were not incremented after simulated territorial intrusions in the laboratory. Plasma levels of cortisol and testosterone were not affected by challenges but were different in wild and captive specimens. Although the endocrine responses to STIs did not differ between intra- and interspecific challenges, agonistic displays expressed by resident fish were more intense towards intraspecific intruders. Taken together, our study emphasizes the need to incorporate androgen precursor concentrations to advance our understanding on the physiology of territorial interactions. Copyright © 2015. Published by Elsevier Inc.
    Hormones and Behavior 04/2015; 71. DOI:10.1016/j.yhbeh.2015.04.011 · 4.51 Impact Factor
  • Nichola J Raihani · Redouan Bshary
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    ABSTRACT: Punishers can benefit from a tough reputation, where future partners cooperate because they fear repercussions. Alternatively, punishers might receive help from bystanders if their act is perceived as just and other-regarding. Third-party punishment of selfish individuals arguably fits these conditions but it is not known whether third-party punishers are rewarded for their investments. Here, we show that third-party punishers are indeed rewarded by uninvolved bystanders. Third-parties were presented with the outcome of a dictator game where the dictator was either selfish or fair and were allocated to one of three treatments where they could choose to do nothing or (i) punish the dictator, (ii) help the receiver or (iii) choose between punishment and helping, respectively. A fourth player ('bystander') then saw the third-party's decision and could choose to reward the third-party or not. Third-parties that punished selfish dictators were more likely to be rewarded by bystanders than third-parties who took no action in response to a selfish dictator. However, helpful third-parties were rewarded even more than third-party punishers. These results suggest that punishment could in principle evolve via indirect reciprocity but also provide insights into why individuals typically prefer to invest in positive actions. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Evolution 03/2015; 69(4). DOI:10.1111/evo.12637 · 4.66 Impact Factor
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    ABSTRACT: Cleaning behavior is known as a classic example of cooperation between unrelated individuals. Although much is known of the behav-ioral processes underlying cooperative behavior, the physiological pathways mediating cooperation remain relatively obscure. Here, we show that altering the activity of serotonin on wild cleaner wrasses Labroides dimidiatus has causal effects on both social and cooperative activities. These cleaners cooperate by removing ectoparasites from visiting " client " reef fishes but prefer to eat client mucus, which constitutes " cheating. " We found that enhancing serotonin made cleaner wrasses more motivated to engage in cleaning behavior and more likely to provide physical contact to clients (tactile stimulation) without spending more time cleaning or cheating more often. Blocking serotonin-mediated response resulted in an apparent decrease in cleaners' cheating levels and in an increase in cleaners' aggressiveness toward smaller conspecifics. Our results provide first evidence that serotonin is a neuromodulatory driver of cooperative behavioral activities and contribute to the understanding of neural pathways of cooperation.
    Behavioral Ecology 03/2015; 26(4). DOI:10.1093/beheco/arv039 · 3.16 Impact Factor
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    Nichola J Raihani · Redouan Bshary
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    ABSTRACT: Humans regularly help strangers, even when interactions are apparently unobserved and unlikely to be repeated. Such situations have been simulated in the laboratory using anonymous one-shot games (e.g., prisoner's dilemma) where the payoff matrices used make helping biologically altruistic. As in real-life, participants often cooperate in the lab in these one-shot games with non-relatives, despite that fact that helping is under negative selection under these circumstances. Two broad explanations for such behavior prevail. The "big mistake" or "mismatch" theorists argue that behavior is constrained by psychological mechanisms that evolved predominantly in the context of repeated interactions with known individuals. In contrast, the cultural group selection theorists posit that humans have been selected to cooperate in anonymous one-shot interactions due to strong between-group competition, which creates interdependence among in-group members. We present these two hypotheses before discussing alternative routes by which humans could increase their direct fitness by cooperating with strangers under natural conditions. In doing so, we explain why the standard lab games do not capture real-life in various important aspects. First, asymmetries in the cost of perceptual errors regarding the context of the interaction (one-shot vs. repeated; anonymous vs. public) might have selected for strategies that minimize the chance of making costly behavioral errors. Second, helping strangers might be a successful strategy for identifying other cooperative individuals in the population, where partner choice can turn strangers into interaction partners. Third, in contrast to the assumptions of the prisoner's dilemma model, it is possible that benefits of cooperation follow a non-linear function of investment. Non-linear benefits result in negative frequency dependence even in one-shot games. Finally, in many real-world situations individuals are able to parcel investments such that a one-shot interaction is turned into a repeated game of many decisions.
    Frontiers in Behavioral Neuroscience 02/2015; 9:39. DOI:10.3389/fnbeh.2015.00039 · 4.16 Impact Factor
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    ABSTRACT: Both latitude and mating system have been proposed to shape relationships between steroid hormone levels and social behavior. Recently it has been postulated that species with long lasting non‐seasonal territorial behavior have low androgen responsiveness. Tropical damselfishes are an ideal family to test this proposition because they show a large variety in mating systems. Here we contribute to the comparative dataset by measuring the response in steroid levels after social modulation in the banded sergeant, Abudefduf septemfasciatus, a species with non‐seasonal territoriality. In highly territorial and broodingmales,we found low androgen and cortisol levels that did not increase after experimental intraspecific simulated territorial intrusions (STI tests). No relationship was found between the variation in steroid hormone levels and territorial responses to naturally occurring territorial intrusions. Although steroid levels were low, male A. septemfasciatus were highly territorial both to STI challenges and to fishes that passed the territory. They often chased intruders for severalmeters away fromthe territory. This indicates that during nest defence in a nonseasonal territorial damselfish species, territorial behaviors are shown independent of variation in androgen and cortisol levels.
    Journal of Experimental Zoology Part A Ecological Genetics and Physiology 02/2015; 323(2). DOI:10.1002/jez.1900 · 1.35 Impact Factor
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    ABSTRACT: Recent work has suggested that punishment is detrimental because punishment provokes retaliation, not cooperation, resulting in lower overall payoffs. These findings may stem from the unrealistic assumption that all players are equal: in reality individuals are expected to vary in the power with which they can punish defectors. Here, we allowed strong players to interact with weak players in an iterated prisoner's dilemma game with punishment. Defecting players were most likely to switch to cooperation if the partner cooperated: adding punishment yielded no additional benefit and, under some circumstances, increased the chance that the partner would both defect and retaliate against the punisher. Our findings show that, in a two-player game, cooperation begets cooperation and that punishment does not seem to yield any additional benefits. Further work should explore whether strong punishers might prevail in multi-player games.
    PLoS ONE 01/2015; 10(1):e0117183. DOI:10.1371/journal.pone.0117183 · 3.23 Impact Factor
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    Nichola J. Raihani · Redouan Bshary
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    ABSTRACT: Punishment is a potential mechanism to stabilise cooperation between self-regarding agents. Theoretical and empirical studies on the importance of a punitive reputation have yielded conflicting results. Here, we propose that a variety of factors interact to explain why a punitive reputation is sometimes beneficial and sometimes harmful. We predict that benefits are most likely to occur in forced play scenarios and in situations where punishment is the only means to convey an individual's cooperative intent and willingness to uphold fairness norms. By contrast, if partner choice is possible and an individual's cooperative intent can be inferred directly, then individuals with a nonpunishing cooperative reputation should typically be preferred over punishing cooperators. Copyright © 2015 Elsevier Ltd. All rights reserved.
    Trends in Ecology & Evolution 01/2015; 30(2). DOI:10.1016/j.tree.2014.12.003 · 15.35 Impact Factor
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    ABSTRACT: 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 cleaner wrasse Labroides dimidiatus. Their 'client' reef fish partners only benefit from interacting if cleaners eat ectoparasites and refrain from gleaning preferred client mucus. 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. Copyright © 2014 Elsevier Inc. All rights reserved.
    Physiology & Behavior 11/2014; 139C:314-320. DOI:10.1016/j.physbeh.2014.11.052 · 3.03 Impact Factor
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    Redouan Bshary · Culum Brown
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    ABSTRACT: The central nervous system, and the brain in particular, is one of the most remarkable products of evolution. This system allows an individual to acquire, process, store and act on information gathered from the environment. The resulting flexibility in behavior beyond genetically coded strategies is a prime adaptation in animals. The field of animal cognition examines the underlying processes and mechanisms. Fishes are a particularly interesting group of vertebrates to study cognition for two reasons (Figure 1). First, they occupy a key position in the vertebrate phylogenetic tree: the common ancestor of the tetrapods was a bony fish. Thus, all vertebrates share key genetic features that code for the body structure, including the vertebrate brain. Similarities in brain structure and function are hence likely to be due to common ancestry. A second reason to study fish cognition is that fish have had their own independent evolution/radiation since they split from tetrapods. Bony fishes are by far the most species-rich vertebrate group. As a consequence, they provide the best options for a comparative approach that aims to link the evolution of cognition to a species’ ecology. Therefore, the study of fishes may reveal general principles of ecological effects on cognitive abilities in vertebrates.
    Current Biology 10/2014; 24(19):R947–R950. DOI:10.1016/j.cub.2014.08.043 · 9.92 Impact Factor
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    Alexander L Vail · Andrea Manica · Redouan Bshary
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    ABSTRACT: Collaborative abilities are integral to human society [1] and their evolutionary origins are of great interest. Chimpanzees are capable of determining appropriately when and with whom to collaborate in a rope-pull experiment [2] - the only non-human species known to possess both abilities. Chimpanzees are thought to share these abilities with humans as a result of common ancestry [2]. Here, we show that a fish - the coral trout Plectropomus leopardus - has partner-choice abilities comparable to those of chimpanzees in the context of its collaborative hunting relationship with moray eels [3]. Using experiments analogous to those performed on chimpanzees [2], but modified to be ecologically relevant to trout, we showed that trout recruit a moray collaborator more often when the situation requires it and quickly learn to choose the more effective individual collaborator. Thus, these collaborative abilities are not specific to apes and may be more closely linked to ecological need [4] than brain size or relatedness to humans.
    Current Biology 09/2014; 24(17):R791-R793. DOI:10.1016/j.cub.2014.07.033 · 9.92 Impact Factor
  • L. Pretot · R. Bshary · S. F. Brosnan
    37th Annual Meeting of the American-Society-of-Primatologists; 09/2014
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    ABSTRACT: Recent 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: a) cortisol, b) glucocorticoid receptor antagonist mifepristone RU486 or c) sham (saline); and observed their cleaning behaviour during the following 45min. 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.
    Hormones and Behavior 06/2014; 66(2). DOI:10.1016/j.yhbeh.2014.06.010 · 4.51 Impact Factor
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    Redouan Bshary · Simon Gingins · Alexander L Vail
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    ABSTRACT: Brain evolution has often been correlated with the cognitive demands of social life. Further progress depends on our ability to link cognitive processes to corresponding brain part sizes and structures, and, ultimately, to demonstrate causality. Recent research suggests that fishes are suitable to test general hypotheses about vertebrate social cognition and its evolution: brain structure and physiology are rather conserved among vertebrates, and fish are able to perform complex decisions in social context. Here, we outline the opportunities for experimentation and comparative studies using fish as model systems, as well as some current shortcomings in fish social cognition research.
    Trends in Cognitive Sciences 05/2014; 18(9). DOI:10.1016/j.tics.2014.04.005 · 21.15 Impact Factor
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    Erica van de Waal · Redouan Bshary · Andrew Whiten
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    ABSTRACT: In the ability and motivation to copy others, social learning has been shown to provide a mechanism for the inheritance of behavioural traditions. Major questions remain about the circumstances and models that shape such social learning. Here, we demonstrate that behavioural food-processing variants among wild vervet monkey, Chlorocebus aethiops, mothers are matched by their infants in their first manipulative approaches to a new foraging problem. In our field experiment, grapes covered with sand were provisioned within groups of wild vervet monkeys that included experienced adults and 17 naïve infants. Monkeys dealt with the dirty food in four different ways. All infants first adopted their mother's way of handling the grapes, rather than those of other mothers or other monkeys eating nearby. Mothers who handled grapes in different ways had infants who were more likely to explore different approaches to handle the sandy grapes. Rarer cases of co-feeding siblings further suggest that copying may occur on the matriline level. Our findings suggest a capacity for detailed copying by infants of their mothers' and matriline members' food-processing techniques when encountering new foods, underlining the significance of familial models in such primate social groups.
    Animal Behaviour 04/2014; 90:41–45. DOI:10.1016/j.anbehav.2014.01.015 · 3.14 Impact Factor
  • S. Gingins · R. Bshary
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    ABSTRACT: Few biological examples of cooperation seem to precisely fit the assumptions of an iterated prisoner’s dilemma. In an attempt to increase biological validity, one model altered the assumption that cooperating is an all-or-nothing decision to a situation where benefits are a function of interaction duration, which in turn is a function of the levels of cooperation. A potential application involves pairs of cleaner fish coinspecting a client fish. In this mutualism, clients visit cleaners to have ectoparasites removed but a conflict of interest exists, as cleaners prefer to eat client mucus, which constitutes cheating. As large clients often flee in response to a cleaner cheating, pair inspections lead to a dilemma: the cheater obtains the benefit while both cleaners share the cost of the client leaving. The model predicts that pairs of cleaners behave more cooperatively toward reef fish clients than when inspecting alone, to entice clients to profit from the increased parasite removal rate and keep interaction duration almost constant. Here, we present field experiments that first replicate results that pairs behave indeed more cooperatively than when inspecting alone and second show that levels of cooperation quantitatively predict the duration of cleaning interactions. We also found that several additional variables may affect the duration of cleaning interactions, such as a client’s willingness to interact with a cleaner, identity of interaction terminator, and the presence of bystanders. In conclusion, introducing benefits as a function of interaction duration into the prisoner’s dilemma framework provides a biologically relevant framework to study cooperation.
    Behavioral Ecology 03/2014; 26(2):350-358. DOI:10.1093/beheco/aru194 · 3.16 Impact Factor
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    ABSTRACT: Deviations from model-based predictions of strategies leading to stable cooperation between unrelated individuals have raised considerable debate in regards to decision-making processes in humans. Here, we present data on cleaner wrasse (Labroides dimidiatus) that emphasize the importance of generalizing this discussion to other species, with the aim to develop a coherent theoretical framework. Cleaners eat ectoparasites and mucus off client fishes and vary their service quality based on a clients’ strategic behaviour. Hitherto, cognitive tasks designed to replicate such behaviour have revealed a strong link between cooperative behaviour and game theoretic predictions. However, we show that individuals from a specific location within our study site repeatedly failed to conform to the published evidence. We started exploring potential functional and mechanistic causes for this unexpected result, focusing on client composition, cleaner standard personality measures and ontogeny. We found that failing individuals lived in a socially simple environment. Decision rules of these cleaners ignored existing information in their environment (‘bounded rationality’), in contrast to cleaners living in a socially complex area. With respect to potential mechanisms, we found no correlations between differences in performance and differences in aggressiveness or boldness, in contrast to results on other cooperative species. Furthermore, juveniles from the two habitat types performed similarly, and better than the adults from the socially simple environment. We propose that variation in the costs and benefits of knowledge may affect a cleaners’ information acquisition and storage, which may explain our observed variation in cooperation and cognition.
    Ethology 03/2014; 120(6). DOI:10.1111/eth.12223 · 1.56 Impact Factor
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    ABSTRACT: Interactions between individuals of different species are commonplace in animal communities. Some behaviors displayed during these interspecific social interactions may be very similar to those displayed during intraspecific social interactions. However, whether functional analogies between intra- and interspecific behaviors translate at the proximate level into an overlap in their underlying endocrine mechanisms remain largely unknown. Because steroids both mediate social behaviors and respond to them, we approached this question by comparing the behavioral and steroid response of free living dusky gregories (Stegastes nigricans [Lacepède, 1802]) to standardized territorial intrusions (sTI) of either conspecific or heterospecific food competitors. S. nigricans is a year-round territorial fish that "cultivates" the algae on which it feeds and is highly aggressive to both intra- and interspecific intruders. Behavioral differences between intra- and interspecific aggressive responses to sTI were marginal, and sTI tests caused an increase in cortisol levels that was positively related with the levels of aggression. In contrast, androgen levels did not increase in response to sTI, yet they showed a positive relationship with agonistic behavior. These results parallel a pattern that was first described for year-round territorial bird species. Furthermore they suggest that changes in endocrine-hormone levels during territoriality might be independent of the species that induces the territorial response.
    Journal of Experimental Biology 02/2014; 217(10). DOI:10.1242/jeb.093666 · 3.00 Impact Factor

Publication Stats

3k Citations
750.22 Total Impact Points


  • 2006–2015
    • Université de Neuchâtel
      • • Institut de biologie (IBIOL)
      • • Laboratoire d'éco-éthologie
      Neuenburg, Neuchâtel, Switzerland
  • 2011
    • ISPA Instituto Universitário
      Lisboa, Lisbon, Portugal
  • 2010
    • University of Queensland
      • School of Biological Sciences
      Brisbane, Queensland, Australia
  • 2002–2005
    • University of Cambridge
      • Department of Zoology
      Cambridge, England, United Kingdom
  • 1997
    • Max Planck Society
      München, Bavaria, Germany