Cleaner Wrasse Research Articles

Cleaner fish coloration decreases predation risk in aggressive fangblenny mimics

Mimicry systems can be classified by the nature of fitness benefits obtained by the mimic, namely increased mating opportunities (reproductive), increased foraging potential (aggressive), or reduced predation risk (protective). However, there is increasing evidence that mimicry categories are not mutually exclusive and mimics can obtain benefits from more than 1 category. Here, I provide evidence that an aggressive mimic, the bluestriped fangblenny Plagiotremus rhinorhynchos, also benefits from reduced predation risk by resembling the juvenile cleaner wrasse Labroides dimidiatus, which are thought to be relatively immune from predation due to the mutualistic nature of cleanerclient interactions. Instead of removing ectoparasites from larger reef fish, bluestriped fangblennies approach and attack reef fish removing scales and dermal tissue. Fangblennies can switch between their mimic and nonmimic coloration within 510min, depending on whether their model (the cleaner wrasse) is present or absent. I found that mimic fangblennies increased their risk-taking behavior toward potential predators compared with nonmimic fangblennies. Mimics were also more likely to attack other reef fish in the presence of predators compared with nonmimics. Animals should only increase risk-taking behavior when they perceive the threat of predation to be low. Therefore, this study provides important evidence that cleaner coloration provides protection from predation to both cleaner fish and their mimics, and the benefits of aggressive mimicry of cleaner wrasse have to be reevaluated in the light of these data.

“Fair” outcomes without morality in cleaner wrasse mutualism

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.

Adult Cleaner Wrasse Outperform Capuchin Monkeys, Chimpanzees and Orang-utans in a Complex Foraging Task Derived from Cleaner – Client Reef Fish Cooperation

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.

Arginine Vasotocin Regulation of Interspecific Cooperative Behaviour in a Cleaner Fish

In 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.

Does Inequity Aversion Motivate Punishment? Cleaner Fish as a Model System

In human social interactions, punishment is often directed at cheating individuals. Subjective reports and neuro-imaging studies indicate that the experience of interacting with a cheat produces negative emotions and that the act of punishing a cheat assuages these feelings. However, while negative emotions may elicit punishment, the precise source of these emotions remains obscure. Specifically, it is often very difficult to tease apart whether punishing individuals are inequity averse (upset because cheating partner receives more than they should) or, more simply, whether they might be loss averse (upset because their payoffs did not meet their expectations). We compare results on punishment and inequity aversion in humans with results from a non-human model system, the cleaning mutualism between bluestreak cleaner wrasse (Labroides dimidiatus) and its reef-fish ‘clients’. Male cleaner fish are known to punish females that cheat during joint client inspections, but a recent study failed to demonstrate evidence for inequity aversion in this species. We suggest that punishment in cleaner fish may be motivated by loss aversion rather than inequity aversion. Punishment in humans might also often be motivated by loss aversion—and empirical studies that disentangle the two competing motives for punishment are a clear research priority.

Mutualistic cleaner fish initiate trait‐mediated indirect interactions by influencing the behaviour of coral predators

1. Indirect interactions resulting from changes in organismal traits such as behaviour [i.e. trait-mediated indirect interactions (TMIIs)] are widespread in biological communities, yet few studies have explored the potential for mutualisms to initiate TMIIs. 2. This study used a combination of behavioural observations and manipulative field experiments to investigate potential TMIIs resulting from a mutualism between specialized cleaner fish and the 'clients' that visit cleaners for the removal of ectoparasites. 3. Behavioural observations indicate that the bluestreak cleaner wrasse, Labroides dimidiatus, increases local predation pressure on corals at cleaner stations by attracting corallivorous butterflyfish to their territories. 4. Observations of the ornate butterflyfish, Chaetodon ornatissimus, suggest a trade-off between seeking cleaning and foraging; individuals decreased their foraging rate at cleaner stations and shifted their diet to include a greater proportion of less preferred prey items. Nonetheless, predation pressure on corals was higher at cleaner stations because the spatial response of butterflyfish to cleaners more than compensated for their lower foraging rates. 5. The results of a field experiment suggest that the greater predation pressure observed at cleaner stations may be sufficient to reduce the growth rate of the unpreferred coral Porites rus. 6. Together, these results emphasize the need to consider mutualists as potential initiators of TMIIs and highlight the importance of integrating individual movement into conceptual analyses of TMIIs.

Reversed sex change by widowed males in polygynous and protogynous fishes: female removal experiments in the field

Sex change, either protogyny (female to male) or protandry (male to female), is well known among fishes, but evidence of bidirectional sex change or reversed sex change in natural populations is still very limited. This is the first report on female removal experiments for polygnous and protogynous fish species to induce reversed sex change in the widowed males in the field. We removed all of the females and juveniles from the territories of dominant males in the cleaner wrasse Labroides dimidiatus (Labridae) and the rusty angelfish Centropyge ferrugata (Pomacanthidae) on the coral reefs of Okinawa. In both species, if new females or juveniles did not immigrate into the territories of the widowed males, some of them emigrated to form male-male pairs. When a male-male pair formed, the smaller, subordinate partner began to perform female sexual behaviours (n = 4 in L. dimidiatus; n = 2 in C. ferrugata) and, finally, released eggs (n = 1, respectively). Thus, the reversed sex change occurred in the widowed males according to the change of their social status. These results suggest that such female removal experiments will contribute to the discovery of reversed sex change in the field also in other polygnous and protogynous species.

Treatment with the glucocorticoid antagonist RU486 reduces cooperative cleaning visits of a common reef fish, the lined bristletooth

Cooperation often involves a conflict of interest. This is particularly true in situations where one individual seeks out a service but cannot properly control the quality of the service given by the partner who would gain from defecting. An example is cleaning mutualism involving the bluestreak cleaner wrasse ( Labroides dimidiatus) and its reef-fish ‘clients’. These cleaners may reduce the stress experienced by their clients by removing parasites; however they occasionally cheat clients (i.e. defect) by eating mucus and other living tissues. Here we present experimental support for the hypothesis that stress responses increase the motivation for clients to seek out such risky asymmetric interactions. We manipulated the stress response by blocking glucocorticoid receptors with the antagonist RU486 in a species that is a regular visitor of cleaner fish, the lined bristletooth ( Ctenochaetus striatus). Field observations 1 week after treatment with RU486 showed that antagonist treatment led to a reduction in cleaning duration compared to control treatment. This was not explained by a general effect on client behavior as intraspecific social behavior appeared unaffected. We propose that antagonist treatment reduced stress responses to the presence of ectoparasites, which in turn reduced the client's perception of benefits from seeking out cleaning interactions. The results demonstrate a hitherto overlooked variable role of stress and stress responses on cooperative behavior.

Cleaner Wrasses Keep Track of the ‘When’ and ‘What’ in a Foraging Task1

In recent years evidence has accumulated that at least some animals can remember the ‘what’, ‘where’ and ‘when’ of personal experiences. Currently, evidence for such ability is taxonomically restricted to birds and mammals. Here, we demonstrate for the first time that cleaner wrasses Labroides dimidiatus are able to remember when they interacted with what after a single event. In nature, cleaners remove ectoparasites from other reef fishes, so-called clients. Clients are depleted, non-stationary food patches at the end of an interaction and replenished only after a delay. In our experiments, we presented twelve cleaners every 2.5 min, a choice between two of a total of four plates with different colours and patterns. One plate was always accessible but contained a non-preferred food item while the other three contained a preferred food item, but allowed a next feeding event only after 5, 10 or 15 min. Thus, to maximise food intake, cleaners had to remember for each choice when they had last interacted with which plate. When confronted with two plates offering preferred food, cleaners showed an overall significant preference for the plate that allowed access during the trial. For six cleaners, the preference was significant. Also, on trials involving the always accessible plate, cleaners discriminated between trials in which they had to eat the non-preferred food and trials on which they could eat the preferred food. In conclusion, cleaners are able to track the ‘when’ and ‘what’ (or possibly ‘who’) within a biologically meaningful time period.

Cleaning wrasse species vary with respect to dependency on the mutualism and behavioural adaptations in interactions

Interspecific mutualisms are an essential feature of life on earth, yet we know little about their evolution and stability. In many mutualisms several species are available as partners, raising questions about the similarity in function and behavioural repertoire depending on the partner species. Furthermore, variation between species in the quantity and quality of interactions resulting in variation in payoffs may allow us to infer the potential evolutionary origin of a multispecies mutualism complex. We addressed these issues in the marine cleaning mutualism, in which so-called ‘cleaners’ remove ectoparasites from so-called ‘client’ reef fish. We measured several parameters concerning the quantity and quality of cleaning interactions in six sympatric cleaner wrasse species. We found significant variation between cleaner species with respect to client diversity, the number of interactions with predatory clients, the duration of interactions, the frequency of client jolts as a correlate of ‘cheating’ by cleaners, and behaviours used for manipulation of client decisions. Exploratory correlations between cleaner species’ dependency and our variables of interest suggest that cleaning originated as a conflict-free by-product mutualism and evolved towards more sophisticated behaviours, including strategic behaviours for interactions with predators, cheating and manipulation specifically adapted to the client type. 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd.

Cleaner wrasse mimics inflict higher costs on their models when they are more aggressive towards signal receivers

Aggressive mimics are predatory species that resemble a 'model' species to gain access to food, mating opportunities or transportation at the expense of a signal receiver. Costs to the model may be variable, depending on the strength of the interaction between mimics and signal receivers. In the Indopacific, the bluestriped fangblenny Plagiotremus rhinorhynchos mimics juvenile cleaner wrasse Labroides dimidiatus. Instead of removing ectoparasites from larger coral reef fish, fangblennies attack fish to feed on scales and body tissue. In this study, juvenile cleaner wrasse suffered significant costs when associated with P. rhinorhynchos mimics in terms of reduced cleaning activity. Furthermore, the costs incurred by the model increased with heightened aggression by mimics towards signal receivers. This was apparently because of behavioural changes in signal receivers, as cleaning stations with mimics that attacked frequently were visited less. Variation in the costs incurred by the model may influence mimicry accuracy and avoidance learning by the signal receiver and thus affect the overall success and maintenance of the mimicry system.

Intraspecific cleaning behaviour of adult cleaner wrasse, Labroides dimidiatus (Perciformes: Labridae)

Here we report on intraspecific cleaning behaviour between two adult bluestreak cleaner wrasse Labroides dimidiatus of similar size on coral reefs surrounding Lizard Island, Great Barrier Reef, Australia. During a SCUBA dive, we observed these individuals posing and the resulting cleaning interactions. While aggression in this species is common between adults of similar size and social class, our observation suggests that these individuals may also cooperate and partially rely on conspecific individuals for cleaning.

Animal Cooperation: Keeping a Clean(ing) Reputation

Cleaner wrasses are a model for the study of animal cooperation. Prospective clients can observe whether the cleaner works faithfully, and cleaners being watched remove just parasites while those that are not, nip the client for a tastier snack.

Long-term effects of the cleaner fish Labroides dimidiatus on coral reef fish communities.

Cleaning behaviour is deemed a mutualism, however the benefit of cleaning interactions to client individuals is unknown. Furthermore, mechanisms that may shift fish community structure in the presence of cleaning organisms are unclear. Here we show that on patch reefs (61–285 m2) which had all cleaner wrasse Labroides dimidiatus (Labridae) experimentally removed (1–5 adults reef−1) and which were then maintained cleaner-fish free over 8.5 years, individuals of two site-attached (resident) client damselfishes (Pomacentridae) were smaller compared to those on control reefs. Furthermore, resident fishes were 37% less abundant and 23% less species rich per reef, compared to control reefs. Such changes in site-attached fish may reflect lower fish growth rates and/or survivorship. Additionally, juveniles of visitors (fish likely to move between reefs) were 65% less abundant on removal reefs suggesting cleaners may also affect recruitment. This may, in part, explain the 23% lower abundance and 33% lower species richness of visitor fishes, and 66% lower abundance of visitor herbivores (Acanthuridae) on removal reefs that we also observed. This is the first study to demonstrate a benefit of cleaning behaviour to client individuals, in the form of increased size, and to elucidate potential mechanisms leading to community-wide effects on the fish population. Many of the fish groups affected may also indirectly affect other reef organisms, thus further impacting the reef community. The large-scale effect of the presence of the relatively small and uncommon fish, Labroides dimidiadus, on other fishes is unparalleled on coral reefs.

Cleaner Wrasses Labroides dimidiatus Are More Cooperative in the Presence of an Audience

Humans may help others even insituations where the recipient will not reciprocate [1-5]. In some cases, such behavior can be explained by the helpers increasing their image score, which will increase the probability that bystanders will help them in the future [5-7]. For other animals, the notion that many interactions take place in an environment containing an audience of eavesdropping bystanders has also been proposed to have important consequences for social behavior, including levels of cooperation [8]. However, experimental evidence is currently restricted to the demonstration that cleaner fish Labroides dimidiatus can learn to solve a foraging task [9]. The cleaners learned to feed against their preference on artificial clients if that allowed them to access additional artificial clients, which would translate into cooperatively eating ectoparasites rather than cheating by eating client mucus under natural conditions [10]. Here we show that cleaners immediately increase current levels of cooperation in the presence ofbystander client reef fish. Furthermore, we find that bystanders respond to any occurrence of cleaners cheating their current client with avoidance. In conclusion, the results demonstrate, for the first time, that image scoring by an audience indeed leads to increased levels of cooperation in a nonhuman animal.

Male cleaner wrasses adjust punishment of female partners according to the stakes

Punishment is an important deterrent against cheating in cooperative interactions. In humans, the severity of cheating affects the strength of punishment which, in turn, affects the punished individual's future behaviour. Here, we show such flexible adjustments for the first time in a non-human species, the cleaner wrasse (Labroides dimidiatus), where males are known to punish female partners. We exposed pairs of cleaners to a model client offering two types of food, preferred 'prawn' items and less-preferred 'flake' items. Analogous to interactions with real clients, eating a preferred prawn item ('cheating') led to model client removal. We varied the extent to which female cheating caused pay-off reduction to the male and measured the corresponding severity of male punishment. Males punished females more severely when females cheated during interactions with high value, rather than low value, model clients; and when females were similar in size to the male. This pattern may arise because, in this protogynous hermaphrodite, cheating by similar-sized females may reduce size differences to the extent that females change sex and become reproductive competitors. In response to more severe punishment from males, females behaved more cooperatively. Our results show that punishment can be adjusted to circumstances and that such subtleties can have an important bearing on the outcome of cooperative interactions.

Oceanic Sharks Clean at Coastal Seamount

Interactions between pelagic thresher sharks (Alopias pelagicus) and cleaner wrasse were investigated at a seamount in the Philippines. Cleaning associations between sharks and teleosts are poorly understood, but the observable interactions seen at this site may explain why these mainly oceanic sharks regularly venture into shallow coastal waters where they are vulnerable to disturbance from human activity. From 1,230 hours of observations recorded by remote video camera between July 2005 and December 2009, 97 cleaner-thresher shark events were analyzed, 19 of which were interrupted. Observations of pelagic thresher sharks interacting with cleaners at the seamount were recorded at all times of day but their frequency declined gradually from morning until evening. Cleaners showed preferences for foraging on specific areas of a thresher shark's body. For all events combined, cleaners were observed to conduct 2,757 inspections, of which 33.9% took place on the shark's pelvis, 23.3% on the pectoral fins, 22.3% on the caudal fin, 8.6% on the body, 8.3% on the head, 2.1% on the dorsal fin, and 1.5% on the gills respectively. Cleaners did not preferentially inspect thresher sharks by time of day or by shark sex, but there was a direct correlation between the amount of time a thresher shark spent at a cleaning station and the number of inspections it received. Thresher shark clients modified their behavior by “circular-stance-swimming,” presumably to facilitate cleaner inspections. The cleaner-thresher shark association reflected some of the known behavioral trends in the cleaner-reef teleost system since cleaners appeared to forage selectively on shark clients. Evidence is mounting that in addition to acting as social refuges and foraging grounds for large visiting marine predators, seamounts may also support pelagic ecology by functioning as cleaning stations for oceanic sharks and rays.

Factors affecting advertising in Indonesian adult and juvenile bluestreak cleaner wrasse (Labroides dimidiatus)

Inter-specific cooperative relationships are important in the behaviour of a variety of animals and often involve a mutually beneficial interaction. This study assessed the behavioural pattern known as ‘advertising’ in the bluestreak cleaner wrasse (Labroides dimidiatus) that remove ectoparasites from other species around Hoga Island, Indonesia. Advertising is the rocking dance that the cleaner performs, which may advertise their services to client fish. The ecological and behavioural factors influencing this behaviour have never been studied despite being of great importance in cleaning interactions. The factors assessed in the present study determined what effects time of day, location, reef position, life stage, client number, client size and interaction duration, had on advertising duration. The significant factors in determining advertising duration were that of life stage, where juveniles advertised significantly more than their adult counterparts (Mann–Whitney U-test: U = 7, p ≤ 0.01, N 1 = 96, N 2 = 96); and reef location (Mann–Whitney U-test: U = 2964.5, p ≤ 0.01, N 1 = 96, N 2 = 96) where cleaning stations on the reef crest exhibited less advertising than on the flat areas for both life stages. Juveniles are likely to advertise more due to the decreased client size and number seen at the juveniles’ stations, as well as the presence of mimics. Reef location is important as the reef crest allows more access to transient clients, hence a reduction in advertising duration. Life stage and location should be explored in future studies as significant factors in the behavioural ecology of cleaner–client interactions.

Short-Term Variation in the Level of Cooperation in the Cleaner Wrasse Labroides dimidiatus: Implications for the Role of Potential Stressors

There is a wealth of game theoretical approaches to the evolution and maintenance of cooperation between unrelated individuals and accumulating empirical tests of these models. This contrasts strongly with our lack of knowledge on proximate causes of cooperative behaviour. Marine cleaning mutualism has been used as a model system to address functional aspects of conflict resolution: client reef fish benefit from cleaning interactions through parasite removal, but cleaner fish Labroides dimidiatus prefer client mucus. Hence, feeding against their preference represents cooperative behaviour in cleaners. Cleaners regularly cheat non-predatory clients while they rarely cheat predatory clients. Here, we asked how precisely cleaners can adjust service quality from one interaction to the next. We found that non-predatory clients receive a better service if the previous client was a predator than if the previous client was a non-predator. In a related laboratory experiment, a hand-net used as a stressor resulted in cleaners feeding more against their preference in subsequent interactions. The combination of the cleaners’ behaviour in the two studies shows that the cleaners’ service quality for a given client species is not fixed, but it can be manipulated. The results suggest that short-term stress is one factor that causes cleaners to increase their levels of cooperation, a hypothesis that is amenable to further experiments manipulating the endocrine system.

Does access to the bluestreak cleaner wrasse Labroides dimidiatus affect indicators of stress and health in resident reef fishes in the Red Sea?

Interactions 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.