[Show abstract][Hide abstract] ABSTRACT: Humans and other animals use previous experiences to make behavioural decisions, balancing the probabilities of receiving rewards or punishments with alternative actions. The dopaminergic system plays a key role in this assessment: for instance, a decrease in dopamine transmission, which is signalled by the failure of an expected reward, may elicit a distinct behavioural response. Here, we tested the effect of exogenously administered dopaminergic compounds on a cooperative vertebrate’s decision-making process, in a natural setting. We show, in the Indo-Pacific bluestreak cleaner wrasse Labroides dimidiatus, that blocking dopamine receptors in the wild induces cleaners to initiate more interactions with and to provide greater amounts of physical contact to their client fish partners. This costly form of tactile stimulation using their fins is typically used to prolong interactions and to reconcile with clients after cheating. Interestingly, client jolt rate, a correlate of cheating by cleaners, remained unaffected. Thus, in low effective dopaminergic transmission conditions cleaners may renegotiate the occurrence and duration of the interaction with a costly offer. Our results provide first evidence for a prominent role of the dopaminergic system in decision-making in the context of cooperation in fish.
Full-text · Article · Feb 2016 · Scientific Reports
[Show abstract][Hide abstract] ABSTRACT: Large disturbances can cause rapid degradation of coral reef communities, but what baseline changes in species assemblages occur on undisturbed reefs through time? We surveyed live coral cover, reef fish abundance and fish species richness in 1997 and again in 2007 on 47 fringing patch reefs of varying size and depth at Mersa Bareika, Ras Mohammed National Park, Egypt. No major human or natural disturbance event occurred between these two survey periods in this remote protected area. In the absence of large disturbances, we found that live coral cover, reef fish abundance and fish species richness did not differ in 1997 compared to 2007. Fish abundance and species richness on patches was largely related to the presence of shelters (caves and/or holes), live coral cover and patch size (volume). The presence of the ectoparasite-eating cleaner wrasse,
, was also positively related to fish species richness. Our results underscore the importance of physical reef characteristics, such as patch size and shelter availability, in addition to biotic characteristics, such as live coral cover and cleaner wrasse abundance, in supporting reef fish species richness and abundance through time in a relatively undisturbed and understudied region.
[Show abstract][Hide abstract] ABSTRACT: Grooming is a key social behavior in many primate species. Research has focused on three important aspects: the short- and long-term trading patterns of grooming for itself and/or for other commodities like tolerance or coalitionary support [1, 2], the issue of whether exchanges are a convincing example for reciprocity [3, 4], and what decision rules underlie trading [5-7]. These issues remain largely unresolved due to the correlative nature of observational studies and the rarity of experimental studies [2, 8-11]. Here, we present a new experimental paradigm to address these questions in wild vervet monkeys (Chlorocebus pygerythrus). Adult females were first trained to approach a personal box, identifiable by unique color patterns, to access high-quality food. During the experiments, two boxes were placed next to each other to induce conflict through forced proximity. We found that while dominants were generally more tolerant toward bonded individuals, recent grooming increased tolerance independently of relationship quality. The latter result shows that vervet monkeys traded grooming for short-term tolerance, where dominants used a direct-reciprocity decision rule. In contrast, females invariably supported the higher-ranking opponent in a conflict, independently of who was the recent grooming partner. Nevertheless, recent grooming increased the probability that a female supported the partner during conflicts with a low-ranking third party. Thus, females' decisions about coalitionary support seem to integrate information about the current social hierarchy with recent grooming events. In conclusion, decision rules underlying trading of grooming for other commodities involve a variety of timescales and factors.
No preview · Article · Nov 2015 · Current biology: CB
[Show abstract][Hide abstract] ABSTRACT: Cheating is a focal concept in the study of mutualism, with the majority of researchers considering cheating to be both prevalent and highly damaging. However, current definitions of cheating do not reliably capture the evolutionary threat that has been a central motivation for the study of cheating. We describe the development of the cheating concept and distill a relative-fitness-based definition of cheating that encapsulates the evolutionary threat posed by cheating, i.e. that cheaters will spread and erode the benefits of mutualism. We then describe experiments required to conclude that cheating is occurring and to quantify fitness conflict more generally. Next, we discuss how our definition and methods can generate comparability and integration of theory and experiments, which are currently divided by their respective prioritisations of fitness consequences and traits. To evaluate the current empirical evidence for cheating, we review the literature on several of the best-studied mutualisms. We find that although there are numerous observations of low-quality partners, there is currently very little support from fitness data that any of these meet our criteria to be considered cheaters. Finally, we highlight future directions for research on conflict in mutualisms, including novel research avenues opened by a relative-fitness-based definition of cheating.
[Show abstract][Hide abstract] ABSTRACT: It is currently widely accepted that the complexity of a species’ social life is a major determinant of its brain complexity, as predicted by the social brain hypothesis. However, it remains a challenge to explain what social complexity exactly is and what the best corresponding measures of brain anatomy are. Absolute and relative size of the brain and of the neocortex have often been used as a proxy to predict cognitive performance. Here, we apply the logic of the social brain hypothesis to marine cleaning mutualism involving the genus Labroides. These wrasses remove ectoparasites from ‘client’ reef fish. Conflict occurs as wrasse prefer client mucus over ectoparasites, where mucus feeding constitutes cheating. As a result of this conflict, cleaner wrasse show remarkable Machiavellian-like behaviour. Using own data as well as available data from the literature, we investigated whether the general brain anatomy of Labroides provides any indication that their Machiavellian behaviour is associated with a more complex brain. Neither data set provided evidence for an increased encephalisation index compared to other wrasse species. Published data on relative sizes of brain parts in 25 species of the order Perciformes suggests that only the diencephalon is relatively enlarged in Labroides dimidiatus. This part contains various nuclei of the social decision making network. In conclusion, gross brain anatomy yields little evidence for the hypothesis that strategic behaviour in cleaning selects for larger brains, while future research should focus on more detailed aspects like the sizes of specific nuclei as well as their cryoarchitectonic structure and connectivity.
[Show abstract][Hide abstract] 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.
[Show abstract][Hide abstract] 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.
Full-text · Article · May 2015 · Behavioral Ecology and Sociobiology
[Show abstract][Hide abstract] 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.
No preview · Article · Apr 2015 · Animal Behaviour
[Show abstract][Hide abstract] 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.
[Show abstract][Hide abstract] ABSTRACT: Cleaning behavior is known as a classic example of cooperation between unrelated individuals. Although much is known of the
behavioral 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.
Full-text · Article · Mar 2015 · Behavioral Ecology
[Show abstract][Hide abstract] 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 versus repeated; anonymous versus 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 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. Finally, 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-li
Full-text · Article · Feb 2015 · Frontiers in Behavioral Neuroscience
[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.
No preview · Article · Feb 2015 · Journal of Experimental Zoology Part A Ecological Genetics and Physiology
[Show abstract][Hide abstract] 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.
[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: 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.