[Show abstract][Hide abstract] 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.
[Show abstract][Hide abstract] 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 10/2014; · 1.61 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Collaborative abilities are integral to human society  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  - 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 . 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 . Using experiments analogous to those performed on chimpanzees , 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  than brain size or relatedness to humans.
Current Biology 09/2014; 24(17):R791-R793. · 9.49 Impact Factor
[Show abstract][Hide abstract] 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; · 3.74 Impact Factor
[Show abstract][Hide abstract] 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; · 16.01 Impact Factor
[Show abstract][Hide abstract] 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.
[Show abstract][Hide abstract] 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.
[Show abstract][Hide abstract] 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; · 3.24 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Mimicry systems are frequently categorized by the type of benefit gained by the mimic's resemblance to its model: protection from threat, including predation (protective mimicry), and increased access to resources, including prey items (aggressive mimicry). These category types may not be mutually exclusive, and some mimics may gain more than one type of benefit. Here we examined a contentious classic textbook example of mimicry between the cleaner wrasse Labroides dimidiatus and its mimic, the sabre-toothed blenny Aspidontus taeniatus. We found that the benefit obtained by the sabre-toothed blenny varied between four geographical locations. At the Great Barrier Reef, in Indonesia and in the Red Sea, it rarely attacked reef fish victims, but instead relied on other food sources such as substrate items, damselfish eggs and tubeworms. Here, the main function of the mimicry system could be to protect the sabre-toothed blenny from predation (protective mimicry) and was consistent with a previous study in Japan. However, in French Polynesia, the sabre-toothed blenny aggressively attacked reef fish frequently, and potential victims were more likely to pose to solicit a cleaning interaction. Diet analysis from individuals in French Polynesia indicated material was gleaned from the surface of fish, including large pieces of fin, implying an increase in the benefits obtained from attacking reef fish (aggressive mimicry). This study provides a potential second example of a mimicry system in which multiple types of benefits are gained by a mimic, and importantly, that the benefits obtained by the mimic vary between different environmental conditions and/or geographical locations. This may have important implications for the maintenance and evolution of mimicry systems and may reflect different stages of an arms race with potential victims.
[Show abstract][Hide abstract] ABSTRACT: The comparative approach provides a powerful tool to study evolutionary questions on both intra- and interspecific variation. It has been applied to a great variety of taxa, including primates. Primate studies differ from those on most other taxa in two ways: first, data from most study sites contain information about only one group. Second, primatologists have used the comparative approach also to identify local traditions, that is, behaviours that spread through social learning. Here, we evaluate the appropriateness of such data by comparing the diet composition of six neighbouring groups of vervet monkeys, Cercopithecus aethiops. We used scan samples to collect diet data, and abundance measures and phenology to assess the availability of the 14 most important tree species utilised during the study. We calculated indices of diet overlap, which were highly variable and could be remarkably low. Furthermore, we found significant differences between group diets with respect to the relative utilisation of 13 of the 14 tree species. For all 13 species, we found positive correlations between local abundance and appearance in the diet, consistent with the importance of local ecology for diet composition. Nevertheless, more detailed comparisons of pairs of groups often revealed significant mismatches between the relative importance of a tree species and its local abundance. In conclusion, local variation merits increased attention by primatologists. While our results are compatible with the possibility that traditions exist on a local (group) rather than population scale, alternative explanations have to be considered.
[Show abstract][Hide abstract] ABSTRACT: The interactions between bacteria and fungi, the main actors of the soil microbiome, remain poorly studied. Here, we show that the saprotrophic and ectomycorrhizal soil fungus Morchella crassipes acts as a bacterial farmer of Pseudomonas putida, which serves as a model soil bacterium. Farming by M. crassipes consists of bacterial dispersal, bacterial rearing with fungal exudates, as well as harvesting and translocation of bacterial carbon. The different phases were confirmed experimentally using cell counting and 13C probing. Common criteria met by other non-human farming systems are also valid for M. crassipes farming, including habitual planting, cultivation and harvesting. Specific traits include delocalization of food production and consumption and separation of roles in the colony (source versus sink areas), which are also found in human agriculture. Our study evidences a hitherto unknown mutualistic association in which bacteria gain through dispersal and rearing, while the fungus gains through the harvesting of an additional carbon source and increased stress resistance of the mycelium. This type of interaction between fungi and bacteria may play a key role in soils.
Proceedings of the Royal Society B: Biological Sciences 10/2013; 280(1773):1-9. · 5.68 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The maintenance of energetically costly flagella by bacteria in water-unsaturated media such as soil still presents an evolutionary conundrum. Potential explanations have focused on rare flooding events allowing dispersal. Such scenarios, however, overlook bacterial dispersal along mycelia as a possible transport mechanism in soils. The hypothesis tested in this study is that dispersal along fungal hyphae may lead to an increase in fitness of flagellated bacteria and thereby propose an alternative explanation for the maintenance of flagella even in unsaturated soils. Dispersal along fungal hyphae was shown for a diverse array of motile bacteria. Additional experiments were conducted in a model system mimicking limited dispersal to measure the fitness effect of dispersal using Pseudomonas putida KT2440 and its non-flagellated isogenic mutant (ΔfliM), in absence or presence of mycelia of Morchella crassipes. In the absence of the fungus, flagellar motility was solely beneficial for conditions of water saturation allowing dispersal, while at conditions limiting dispersal the non-flagellated mutant exhibited a higher fitness than the wild type strain. By contrast, in the presence of a mycelial network at conditions limiting dispersal, the flagellated strain was able to disperse using the mycelial network and had a higher fitness than the mutant. Our results propose that the benefit of mycelia associated dispersal contributes to explaining the persistence of flagellar motility in water-unsaturated environments.
Applied and Environmental Microbiology 08/2013; · 3.95 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 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 Indo-Pacific 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.
[Show abstract][Hide abstract] ABSTRACT: Discussions about social behavior are generally limited to fitness effects of interactions occurring between conspecifics. However, many fitness relevant interactions take place between individuals belonging to different species. Our detailed knowledge about the role of hormones in intraspecific interactions provides a starting point to investigate how far interspecific interactions are governed by the same physiological mechanisms. Here, we carried out standardized resident-intruder (sRI) tests in the laboratory to investigate the relationship between androgens and both intra- and interspecific aggression in a year-round territorial coral reef fish, the dusky gregory, Stegastes nigricans. This damselfish species fiercely defend cultivated algal crops, used as a food source, against a broad array of species, mainly food competitors, and thus represent an ideal model system for comparisons of intra-and interspecific territorial aggression. In a first experiment, resident S. nigricans showed elevated territorial aggression against intra- and interspecific intruders, yet neither elicited a significant increase in androgen levels. However, in a second experiment where we treated residents with flutamide, an androgen receptor blocker, males but not females showed decreased aggression, both towards intra- and interspecific intruders. Thus androgens appear to affect aggression in a broader territorial context where species identity of the intruder appears to play no role. This supports the idea that the same hormonal mechanism may be relevant in intra- and interspecific interactions. We further propose that in such a case, where physiological mechanisms of behavioral responses are found to be context dependent, interspecific territorial aggression should be considered a social behavior.
Hormones and Behavior 07/2013; · 3.74 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The insight that animals’ cognitive abilities are linked to their evolutionary history, and hence their ecology, provides the framework for the comparative approach. Despite primates renowned dietary complexity and social cognition, including cooperative abilities, we here demonstrate that cleaner wrasse outperform three primate species, capuchin monkeys, chimpanzees and orang-utans, in a foraging task involving a choice between two actions, both of which yield identical immediate rewards, but only one of which yields an additional delayed reward. The foraging task decisions involve partner choice in cleaners: they must service visiting client reef fish before resident clients to access both; otherwise the former switch to a different cleaner. Wild caught adult, but not juvenile, cleaners learned to solve the task quickly and relearned the task when it was reversed. The majority of primates failed to perform above chance after 100 trials, which is in sharp contrast to previous studies showing that primates easily learn to choose an action that yields immediate double rewards compared to an alternative action. In conclusion, the adult cleaners’ ability to choose a superior action with initially neutral consequences is likely due to repeated exposure in nature, which leads to specific learned optimal foraging decision rules.
[Show abstract][Hide abstract] ABSTRACT: In humans, referential gestures intentionally draw the attention of a partner to an object of mutual interest, and are considered a key element in language development. Outside humans, referential gestures have only been attributed to great apes and, most recently, ravens. This was interpreted as further evidence for the comparable cognitive abilities of primates and corvids. Here we describe a signal that coral reef fishes, the grouper Plectropomus pessuliferus marisrubri and coral trout Plectropomus leopardus, use to indicate hidden prey to cooperative hunting partners, including giant moray eels Gymnothorax javanicus, Napoleon wrasses Chelinus undulatus and octopuses Octopus cyanea. We provide evidence that the signal possesses the five attributes proposed to infer a referential gesture: it is directed towards an object, mechanically ineffective, directed towards a potential recipient, receives a voluntary response and demonstrates hallmarks of intentionality. Thus, referential gesture use is not restricted to large-brained vertebrates.
[Show abstract][Hide abstract] ABSTRACT: Baumard et al. propose a functional explanation for the evolution of a sense of fairness in humans: Fairness preferences are advantageous in an environment where individuals are in strong competition to be chosen for social interactions. Such conditions also exist in nonhuman animals. Therefore, it remains unclear why fairness (equated with morality) appears to be properly present only in humans.
Behavioral and Brain Sciences 02/2013; 36(1):83-4. · 18.57 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The Machiavellian/Social Intelligence Hypothesis proposes that a complex social environment selected for advanced cognitive abilities in vertebrates. In primates it has been proposed that sophisticated social strategies like obtaining suitable coalition partners are an important component of social intelligence. Knowing the rank relationships between group members is a basic requirement for the efficient use of coalitions and the anticipation of counter-coalitions. Experimental evidence for such knowledge currently exists in only few species. Here, we conducted rank reversal playback experiments on adult females belonging to three different groups of free-ranging vervet monkeys (Chlorocebus aethiops pygerythrus) to test their knowledge of the female hierarchy. Playbacks simulating rank reversals (subordinate aggressing a dominant) induced longer looking times than playbacks simulating a dominant aggressing a subordinate. Vervet monkey females therefore seem to compute the rank relationships between other females. Our results suggest that detailed social knowledge about rank relationships may be widespread in primates and potentially also in other species living in stable groups.
PLoS ONE 01/2013; 8(3):e58562. · 3.53 Impact Factor