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.     

Cleaner fish, Labroides dimidiatus, diet preferences for different types of mucus and parasitic gnathiid isopods

Cleaner fish, Labroides dimidiatus, prefer the mucus of the parrotfish, Chlorurus sordidus, to parasitic gnathiid isopods, the main items in their diet, indicating a major conflict between clients and cleaners over what the latter should eat during interactions. We tested whether the conflict varied with client species (and the quality of its mucus) and with the presence of blood in the gnathiids. First, we offered cleaners the choice between mucus of the parrotfish and that of the snapper, Lutjanus fulviflamma. When offered equal amounts of mucus on Plexiglas plates, cleaners readily developed a significant preference for the parrotfish mucus. Reducing the amount of parrotfish mucus by 75% made the preference disappear. In a second test, we offered the cleaners gnathiids that were or were not engorged with client fish blood. Cleaners showed no significant preference for either food item. Our results suggest that the degree of conflict between cleaners and clients may vary between species, depending on whether the latter have a preferred mucus. In contrast, the cleaners' lack of preference for engorged gnathiids benefits clients because it means that cleaners do not hesitate to eat unengorged gnathiids before the gnathiids harm the fish by removing blood or by transmitting blood parasites.     

Punishment and partner switching cause cooperative behaviour in a cleaning mutualism

What are the mechanisms that prevent partners from cheating in potentially cooperative interactions between unrelated individuals? The cleaner fish Labroides dimidiatus and client reef fish both benefit from an interaction as long as the cleaner eats ectoparasites. However, the cleaner fish prefers some client mucus, which constitutes cheating. Field observations suggested that clients control such cheating by using punishment (chasing the cleaner) or by switching partners (fleeing from the cleaner). Here, we tested experimentally whether such client behaviours result in cooperative cleaner fish. Cleaners were allowed to feed from Plexiglas plates containing prawn items and fish flake items. A lever attached to the plates allowed us to mimic the behaviours of clients. As cleaners showed a strong preference for prawn over flakes, we taught them that eating their preferred food would cause the plate to either chase them or to flee, while feeding on flakes had no negative consequences. We found a significant shift in cleaner fish foraging behaviour towards flake feeding after six learning trials. As punishment and terminating an interaction resulted in the cleaners feeding against their preferences in our experiment, we propose that the same behaviours in clients improve the service quality of cleaners under natural conditions.     

Variation in Cleaner Wrasse Cooperation and Cognition: Influence of the Developmental Environment?

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.     

Geographic Variation in the Behaviour of the Cleaner Fish Labroides dimidiatus (Labridae)

Geographical variation in the outcome of interspecific interactions has a range of proximate ecological causes. For instance, cleaning interactions between coral reef fishes can result in benefits for both the cleaner and its clients. However, because both parties can cheat and because the rewards of cheating may depend on the local abundance of ectoparasites on clients, the interaction might range from exploitative to mutualistic. In a comparative analysis of behavioural measures of the association between the cleaner fish Labroides dimidiatus and all its client species, we compared cleaning interactions between two sites on the Great Barrier Reef that differ with respect to mean ectoparasite abundance. At Heron Island, where client fish consistently harbour fewer ectoparasites, client species that tended to pose for cleaners were more likely to receive feeding bites by cleaners than client species that did not pose for cleaners. This was not the case at Lizard Island, where ectoparasites are significantly more abundant. Client fish generally spent more time posing for cleaners at Lizard Island than their conspecifics at Heron Island. However, fish at Heron Island were inspected longer on average by cleaners than conspecifics at Lizard Island, and they incurred more bites and swipes at their sides per unit time from cleaners. These and other differences between the two sites suggest that the local availability of ectoparasites as a food source for cleaners may determine whether clients will seek cleaning, and whether cleaners will feed on parasites or attempt to feed on client mucus. The results suggest that cleaning symbiosis is a mosaic of different outcomes driven by geographical differences in the benefits for both participants.     

Cleaner wrasse prefer client mucus: support for partner control mechanisms in cleaning interactions

Recent studies on cleaning behaviour suggest that there are conflicts between cleaners and their clients over what cleaners eat. The diet of cleaners usually contains ectoparasites and some client tissue. It is unclear, however, whether cleaners prefer client tissue over ectoparasites or whether they include client tissue in their diet only when searching for parasites alone is not profitable. To distinguish between these two hypotheses, we trained cleaner fish Labroides dimidiatus to feed from plates and offered them client mucus from the parrotfish Chlorurus sordidus, parasitic monogenean flatworms, parasitic gnathiid isopods and boiled flour glue as a control. We found that cleaners ate more mucus and monogeneans than gnathiids, with gnathiids eaten slightly more often than the control substance. Because gnathiids are the most abundant ectoparasites, our results suggest a potential for conflict between cleaners and clients over what the cleaner should eat, and support studies emphasizing the importance of partner control in keeping cleaning interactions mutualistic.     

Choosy reef fish select cleaner fish that provide high-quality service

Reef fish that actively visit cleaner fish to have parasites and dead or infected tissue removed face two potential problems: they might have to wait while cleaners inspect other clients, and cleaners might feed on healthy body tissue, a behaviour that is referred to as cheating. Individuals of some ‘client’ species have large home ranges, which cover several cleaning stations, while others have small territories or home ranges with access to only one cleaning station. The former can thus choose between cleaners, while the latter cannot. We investigated whether clients with large home ranges change cleaning partners to outplay cleaners against each other to achieve (1) priority of access over clients with no choice at cleaning stations and (2) control over cheating by cleaners. We followed individuals of longnosed parrotfish, Hipposcarus harid, for up to 120 min in their natural environment and noted their interactions with cleaner wrasses, Labroides dimidiatus. Individuals were likely to return to the same cleaning station if the previous interaction had ended without conflict but changed cleaners for the next inspection if they had been either cheated or ignored, at least if the time between two consecutive visits was short. The overall attractiveness of a cleaning station seemed to be largely independent of service quality, which appeared to be similar at all stations. This is the first empirical evidence that the option to change partners is used as a control mechanism to stabilize cooperative behaviour.     

Asymmetric cheating opportunities and partner control in a cleaner fish mutualism

How can cooperation persist if, for one partner, cheating is more profitable than cooperation in each round, while the other partner has no option to cheat? Our laboratory experiments suggest that such a situation exists between the cleaner fish Labroides dimidiatus and its nonpredatory client reef fish species, which actively seek cleaners to have their ectoparasites removed. Clients Ctenochaetus striatus regularly jolted in response to cleaner mouth contact, and these jolts were not linked to the removal of parasites. In addition, cleaners did not search for parasites but fed on mucus when exposed to anaesthetized clients, which could not control the cleaners' behaviour. Field data showed that clients often terminated an interaction immediately after a jolt. Client species with access to only one cleaning station, owing to their small territories or home ranges, terminated interactions mainly by chasing cleaners while clients with access to two or more cleaning stations mainly swam away. Thus, the chasing of cleaners appeared to be a form of punishment, imposing costs on the cleaner at the client's (momentary) expense. Chasing yields future benefits, as jolts were on average less frequent during interactions between cleaners and individuals that had terminated their previous interaction by aggressive chasing.     

Ontogenetic shift in host tolerance controls initiation of a cleaning symbiosis

When the interests of mutualists are not perfectly aligned, control mechanisms that modulate interactions can maintain mutually beneficial outcomes and stabilize mutualisms over evolutionary time. However, the costs and benefits of symbiosis often change with ontogeny and whether control mechanisms are adjusted to reflect ontogenetic changes is largely unknown. We examined the recently described cleaning symbiosis between crayfish Cambarus chaugaensis and ectosymbiotic annelids (Xironodrilus appalachius) for evidence of ontogenetic changes in symbiont control. Xironodrilus appalachius provide a beneficial cleaning service to C. chaugaensis by removing epibiotic accumulations from the gills, but crayfish also incur costs via density‐dependent facultative parasitism of gill tissue. A series of laboratory experiments using crayfish from three size (age) – classes demonstrated that crayfish use grooming to limit cleaner density and grooming effects on cleaners varied with crayfish age. Small crayfish quickly removed essentially all of their cleaners. Intermediate crayfish removed most of their cleaners, but some cleaners persisted at a location apparently inaccessible to grooming and far from the gill chamber. Large crayfish removed a smaller proportion of cleaners and cleaners were allowed access to the gill chamber, thus initiating the cleaning symbiosis. Cleaner removal was not dependent on cleaner density, suggesting that crayfish do not regulate cleaners to a specific density. Experimental results were corroborated by patterns observed during a field survey. We argue decreased cleaner removal and relaxed control of cleaner attachment sites corresponds to ontogenetic changes in the costs and benefits of symbiosis. This study integrates two major theoretical perspectives from ecological literature; control mechanisms and ontogenetic shifts, and illustrates how changes in control mechanisms with ontogeny may favor life‐long positive outcomes of symbiosis. Ontogenetic shifts in the costs and benefits of symbiosis may be common; therefore future theoretical and empirical studies of symbioses should incorporate both perspectives.     

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.     

A comparative study of cleaning activity of two reef fishes at Fernando de Noronha Archipelago,tropical West Atlantic

Cleaner fishes are usually classified as obligate or facultative cleaners according to their diet and the extent to which their nutritional requirements in the different ontogenetic stages are gained from cleaning. While obligate cleaners clean throughout their lives and ingest mainly food taken from the clients’ body surface, facultative cleaners clean only as juveniles and have a broader diet. In addition, some facultative cleaners may experience a relatively higher predation risk, and thus rarely interact with piscivorous fishes. Despite these acknowledged differences, there are very few studies that compare cleaning activity of obligate and facultative cleaners within the same area. Cleaning activity of the obligate cleaner goby Elacatinus cf. randalli and the facultative cleaner wrasse Thalassoma noronhanum were comparatively examined at Fernando de Noronha Archipelago, tropical West Atlantic. The client assemblage attended by the two cleaners differed, as the goby attended a slightly greater diversity of species (22), mostly piscivores and zoobenthivores, and the wrasse attended fewer species (19), mostly planktivores. Chromis multilineata was the most common client species of both cleaners, although body size (which is expected to be positively correlated to clients’ ectoparasite load) of C. multilineata individuals attended by the goby was larger than that of the individuals attended by the wrasse. Despite such differences, T. noronhanum showed a surprisingly species-rich client assemblage when compared with other cleaners of the genus Thalassoma. In addition, the frequency and time spent on cleaning interactions, as well as the number of client species attended per 10-min period, was similar for both cleaner species, which indicate that they have important yet complimentary ecological roles in the reef community at Fernando de Noronha Archipelago.     

Biting cleaner fish use altruism to deceive image-scoring client reef fish

Humans are more likely to help those who they have observed helping others previously. Individuals may thus benefit from being altruistic without direct reciprocity of recipients but due to gains in 'image' and associated indirect reciprocity. I suggest, however, that image-scoring individuals may be exploitable by cheaters if pay-offs vary between interactions. I illustrate this point with data on cleaner-client reef fish interactions. I show the following: (i) there is strong variation between cleaners with respect to cheating of clients (i.e. feeding on client tissue instead of parasites); (ii) clients approach cleaners, that they observe cooperating with their current client and avoid cleaners that they observe cheating; (iii) cleaners that cheat frequently are avoided more frequently than more cooperative cleaners (iv) cleaners that cheat frequently behave altruistically towards their smallest client species; (v) altruistic acts are followed by exploitative interactions. Thus, it appears that cleaners indeed have an image score, which selects for cooperative cleaners. However, cheating cleaners use altruism in potentially low-pay-off interactions to deceive and attract image-scoring clients that will be exploited.     

Caribbean Cleaning Gobies Prefer Client Ectoparasites Over Mucus

If cooperation often involves investment, then what specific conditions prevent selection from acting on cheaters that do not invest? The mutualism between the Indo‐Pacific cleaner wrasse Labroides dimidiatus and its reef fish clients has been a model system to study conflicts of interest and their resolution. These cleaners prefer client mucus over ectoparasites – that is, they prefer to cheat – but punishment and partner switching by clients enforce cooperative behaviour by cleaners. By contrast, clients of Caribbean cleaning gobies (Elacatinus spp.) do not to use punishment or partner switching. Here, we test the hypothesis that the behavioural differences between these two cleaner fish systems are caused by differences in cleaner foraging preferences. In foraging choice experiments, we offered broadstripe cleaning gobies Elacatinus prochilos client‐derived parasitic isopods, client mucus and a control food item. The cleaning gobies significantly preferred ectoparasites over mucus or the control item, which contrasts with cleaner wrasses. We propose that the low level of cleaner–client conflict arising from cleaning goby foraging preferences explains the observed lack of strategic partner control behaviour in the clients of cleaning gobies.     

Cleaner wrasses Labroides dimidiatus are more cooperative in the presence of an audience

Humans may help others even in?situations 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 of?bystander 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.     

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.     

Cleaner fish Labroides dimidiatus manipulate client reef fish by providing tactile stimulation.

The cleaner wrasse Labroides dimidiatus often touches 'client' reef fish dorsal fin areas with its pelvic and pectoral fins. The relative spatial positions of cleaner and client remain constant and the cleaner's head points away from the client's body. Therefore, this behaviour is not compatible with foraging and the removal of client ectoparasites. As clients seek such 'tactile stimulation', it can be classified as an interspecific socio-positive behaviour. Our field observations on 12 cleaners (observation time of 112h) suggest that cleaners use tactile stimulation in order to successfully (i) alter client decisions over how long to stay for an inspection, and (ii) stop clients from fleeing or aggressive chasing of the cleaner in response to a cleaner fish bite that made them jolt. Finally, predatory clients receive tactile stimulation more often than non-predatory clients, which might be interpreted as an extra service that cleaners give to specific partners as pre-conflict management, as these partners would be particularly dangerous if they started a conflict. We therefore propose that cleaner fish use interspecific social strategies, which have so far been reported only from mammals, particularly primates.     

Hospital Trash: Cleaners Speak of Their Role in Disease Prevention

Feminist researchers have contrasted the caring provided by women in hospitals with a more fragmented "curing" approach, which they identify with the predominantly male professions of medicine and surgery. The author spoke with hospital cleaners about their jobs and their health. Several themes emerged: the invisibility of the cleaning function, lack of respect for cleaners, representations of cleaning as undemanding, and assumptions that women s work in cleaning is particularly easy. Cleaners use various strategies to combat these stereotypes but receive little help from administrators or fellow employees. There is a hierarchy in the status of Quebec hospital workers with curing (doctors) at the top, followed by caring and healing (nurses, therapists, and attendants), and hygiene (cleaners, sterilizers, and launderers) at the bottom. Authority hierarchies in health care are not related to gender in a simple way, although there is discrimination against women cleaners. The fact that cleaning, especially cleaning performed by women, is invisible to managers, other hospital personnel, and patients has important consequences for cleaners' and for patients' health. [cleaning, health, hierarchy, hospital workers, gender]     

Colourful stripes send mixed messages to safe and risky partners in a diffuse cleaning mutualism

The steps by which neutral, random and/or negative biological interactions evolve into mutualistic ones remain poorly understood. Here, we study Elacatinus gobies and the ‘client’ fishes they clean. Colourful stripes are common to mutualist cleaners and noncleaning sister species. Blue stripes are unique to cleaners and are more conspicuous to predators than are basal yellow or green stripes. In turn, we focused on the role of colour as a potentially specialized signal. We show that cleaners may possess a chemical defence and demonstrate that stripes are sufficient to elicit client posing behaviour and to deter attack, corroborating the putative role of chemistry. Analysis of previously published records shows that yellow cleaners interact with predatory clients less often compared to green and blue cleaners. Our results highlight evolution from predator resistance to advertising with conspicuous signals. Similar trajectories, via recognizable signals to risky partners, may be common in other diffuse mutualisms.     

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 Activity of Juvenile Angelfish, Pomacanthus paru, on the Reefs of the Abrolhos Archipelago, Western South Atlantic

Studies on fish cleaning symbiosis in the tropical western Atlantic concentrate on specialized cleaner gobies and wrasses. On the reefs of the Abrolhos Archipelago, off the eastern Brazilian coast, juvenile french angelfish, Pomacanthus paru, clean a rich and varied community of fish clients. We recorded 31 reef fish species, including large predators such as groupers, jacks, and morays, being serviced by the french angelfish on cleaning stations situated mostly on seagrass flats. The angelfish performs a characteristic fluttering swimming at the station and, during cleaning events, touches the body of the clients with its pelvic fins. Frequency of encounters between the cleaner and its clients do not reflect the local abundance of client species; most of these move from the reefs to the sand flats to be cleaned. We found no correlation between client size and duration of cleaning events. The conspicuous black and yellow pattern, the fluttering swimming, the tenure of cleaning stations, the physical contact with the client, and the varied community of clients, qualify the juveniles of P. paru as specialized cleaners comparable to the gobies of the genus Elacatinus.