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.     

The Meaning of Jolts by Fish Clients of Cleaning Gobies

Cooperative interactions offer the inherent possibility of cheating by each of the interacting partners. A key challenge to behavioural observers is to recognize these conflicts, and find means to measure reliably cheating in natural interactions. Cleanerfish Labroides dimidiatus cheat by taking scales and mucus from their fish clients and such dishonest cleaning has been previously recognized in the form of whole‐body jolts by clients in response to cleaner mouth contact. In this study, we test whether jolts may be a general client response to cheating by cleaners. We experimentally varied the ectoparasite loads of yellowtail damselfish (Microspathodon chrysurus), a common client of the cleaning goby Elacantinus evelynae, and compared the rates of jolts on parasitized and deparasitized clients. As predicted if jolts represent cleaner cheating, deparasitized clients jolted more often than parasitized clients, and overall jolt rates increased over time as client parasite load was presumably reduced by cleaning activity. Yellowtail damselfish in the wild jolted significantly less frequently than those in captivity, which is consistent with a loss of ectoparasites during capture. Our results suggest that jolts by clients of cleaning gobies are not related to the removal of ectoparasites. Client jolts may therefore be a generally accurate measure of cheating by cleanerfish.     

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 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.     

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.     

Cleaner fish use tactile dancing behavior as a preconflict management strategy

The most commonly asked question about cooperative interactions is how they are maintained when cheating is theoretically more profitable. In cleaning interactions, where cleaners remove parasites from apparently cooperating clients, the classical question asked is why cleaner fish can clean piscivorous client fish without being eaten, a problem Trivers used to explain reciprocal altruism. Trivers suggested that predators refrain from eating cleaners only when the repeated removal of parasites by a particular cleaner results in a greater benefit than eating the cleaner. Although several theoretical models have examined cheating behavior in clients, no empirical tests have been done (but see Darcy ). It has been observed that cleaners are susceptible to predation. Thus, cleaners should have evolved strategies to avoid conflict or being eaten. In primates, conflicts are often resolved with conflict or preconflict management behavior. Here, I show that cleaner fish tactically stimulate clients while swimming in an oscillating "dancing" manner (tactile dancing) more when exposed to hungry piscivorous clients than satiated ones, regardless of the client's parasite load. Tactile dancing thus may function as a preconflict management strategy that enables cleaner fish to avoid conflict with potentially "dangerous" clients.     

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.     

The cost of cleanerfish mimics to their models

In aggressive mimicry, a 'predatory' species resembles a model that is harmless or beneficial to a third species, the 'dupe'. Perhaps the most extraordinary case of aggressive mimicry occurs in Indo‐Pacific cleaning symbioses, where cleaner wrasses (the models) remove ectoparasites from larger fish clients. Several species of fangblennies mimic cleaners in behaviour and coloration. Instead of removing ectoparasites, however, fangblennies tear off fins, skin and scales from unsuspecting clients (the dupes). There is some debate over the extent to which cleanerfish mimics are really mimics because in some populations, the contribution of fish tissue to fangblenny diet is limited. In this study, I examine the impact of the resemblance between bluestriped fangblennies ( Plagiotremus rhinorhynchus ) and its putative model, the juvenile bluestreak cleaner wrasse ( Labroides dimidiatus ), on the model's cleaning activity to test the theoretical prediction that mimics should decrease the fitness of their models. I show that the presence of a bluestripe fangblenny in the vicinity of cleaner wrasses results in significantly lower client visit rates and inspection times compared to cleaners without a fangblenny nearby, and discuss why cleaner wrasses tolerate mimics near cleaning stations.     

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.     

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.     

Degrees of honesty: cleaning by the redlip cleaner wrasse Labroides rubrolabiatus

Cleaning symbioses among coral reef fishes are highly variable. Cleanerfishes vary in how much they cooperate with (i.e. remove only ectoparasites) or cheat (i.e. bite healthy tissue, scales or mucus) on their fish clients. As a result, clients use various strategies to enforce cooperation by cleaners (e.g. punishment or partner choice), and cleaners use tactile stimulation to manipulate cheated client behaviour. We provide the first detailed observations of cleaning behaviour of the redlip cleaner wrasse Labroides rubrolabiatus and ask where interactions with this cleanerfish lie on the continuum of cleanerfish honesty, client control, and cleanerfish manipulation. Ninety per cent of redlip cleaner wrasses took jolt-inducing cheating bites from their clients, but they did so at a very low rate (~ 2 jolts per 100 s inspection). Retaliatory chases by clients were uncommon. Three-quarters (30 of 40) of cleaner wrasses used tactile stimulation on their clients, but rarely did so to reconcile with cheated clients. Instead, the majority (70%) of tactile stimulation events targeted a passing client that then stopped for inspection. The relationship between redlip cleaner wrasses and their clients appears to be less conflictual than those documented in other Labroides cleanerfishes. Future studies should test whether this low level of conflict is consistent across space and time and is underpinned by a preference for ectoparasites over other client-gleaned items. As an active cleaner that appears to take few cheating bites from their clients, L. rubrolabiatus has the potential to be as important a driver of fish health and community structure on coral reefs as its better-known relatives.

     

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.     

Cleaner shrimp use a rocking dance to advertise cleaning service to clients

Signals transmit information to receivers about sender attributes, increase the fitness of both parties, and are selected for in cooperative interactions between species to reduce conflict [1, 2]. Marine cleaning interactions are known for stereotyped behaviors [3-6] that likely serve as signals. For example, "dancing" and "tactile dancing" in cleaner fish may serve to advertise cleaning services to client fish [7] and manipulate client behavior [8], respectively. Cleaner shrimp clean fish [9], yet are cryptic in comparison to cleaner fish. Signals, therefore, are likely essential for cleaner shrimp to attract clients. Here, we show that the yellow-beaked cleaner shrimp [10] Urocaridella sp. c [11] uses a stereotypical side-to-side movement, or "rocking dance," while approaching potential client fish in the water column. This dance was followed by a cleaning interaction with the client 100% of the time. Hungry cleaner shrimp, which are more willing to clean than satiated ones [12], spent more time rocking and in closer proximity to clients Cephalopholis cyanostigma than satiated ones, and when given a choice, clients preferred hungry, rocking shrimp. The rocking dance therefore influenced client behavior and, thus, appears to function as a signal to advertise the presence of cleaner shrimp to potential clients.     

Fish cleaning behaviour of shrimp

Cleaning behaviour of five species of shrimp from three families was studied at three different geographic locations in an effort to gain a quantitative understanding of cleaning behaviour, and to compare a broad cross-section of cleaner shrimp species. Two shrimp from the genus Periclimenes , two from the genus Lysmata , and one from the genus Stenopus were used and 27 hours of recorded laboratory observations were made for each of the five shrimp species.
All shrimp species were inactive most of the observed time, and most spent less than 2% of the observed time cleaning fish hosts. Also, the shrimp spent more time cleaning the ventral rather than the dorsal surface of the fish because they were reluctant to board the fish. However, evenness in cleaning does not appear to be an indicator of overall excellence in cleaning because the two best cleaners (based on number and duration of cleaning bouts) were among the least even in their cleaning.
The fish cleaning behaviour of the shrimp appeared to be strictly stereotypic in form, but the stimulus-response and the total amount of cleaning differed greatly among the five species. A Cleaning Efficiency Index (CEI) was created in an attempt to incorporate significant aspects of the cleaning behaviour. According to this CEI, Lysmata grabhami was by far the most efficient (best) cleaner, CEI = 55–51, compared to the others; Stenopus hispidus , 33–78; Periclimenes pedersoni , 6–29; Periclimenes yucatunicus , 5–60; and Lysmata californien , 2–12.
The cleaners most widely distributed geographically have the highest CEI scores, while the most localized cleaners have the lowest CEIs. This relationship may allow the CEI score to be useful in determining a cleaner shrimp's potential geographical distribution, and may also serve as an indicator for the degree of phylogenetic relationship to other cleaner shrimps.     

Does Competition for Clients Increase Service Quality in Cleaning Gobies?

In a biological market, members of one trading class try to outbid each other to gain access to the most valuable partners. Competition within class can thus force individuals to trade goods or services more cheaply, ultimately resulting in conflict (e.g. cheating) over the value of commodities. Cleaning symbioses among fish appear to be good examples of biological markets. However, the existence and effect of outbidding competition among either types of traders (cleaners or clients) have never been tested. We examined whether increasing competition among cleaning gobies ( Elacatinus spp.) for access to clients results in outbidding in the form of provision of a better cleaning service. On reefs where fish clients visited cleaning stations less frequently, and thus competition among cleaners was higher, cleaning gobies ingested fewer scales relative to the number of ingested parasites, i.e. they cleaned more honestly. This shift in cleaner behaviour towards greater honesty is consistent with a greater market value of access to clients in the face of competition among cleaners. However, this pattern could have also arisen as a result of differences in ectoparasite availability across reefs and therefore in value of the commodity offered by clients. Experimental manipulations will be required to determine whether cleaning service quality by cleaning gobies was enhanced solely because of competitive outbidding.     

In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish

Although cleaning interactions are deemed a textbook example of mutualism, there is limited evidence that clients benefit from cleaning in terms of reduced ectoparasite loads. The proximate causes of cleaning behaviour are also contentious. We examined the effect of ectoparasite load (i.e. the number of larval gnathiid isopods) on client behaviour under natural conditions. Diel variation in gnathiid loads of longfin damselfish, Stegastes diencaeus, a common coral reef fish client of cleaning gobies (Elacatinus spp.), was correlated with variation in gnathiid emergence from the substratum at sites in both Puerto Rico and St John, northeastern Caribbean. Both benthic emergence of gnathiids and their infestation on damselfish peaked in the morning. Concomitantly, clients spent significantly more time posing for and being inspected by cleaners in the morning than at other times of day. Our results corroborate recent experimental results on captive clients and are consistent with the mutualistic interpretation of cleaning symbioses.     

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.     

Cleaner fish become hosts: a novel form of parasite transmission

Adult bucephalid trematodes (Digenea) generally only occur in piscivorous fish. Within labrid fishes they are very rare, however, we have found them in labrid cleaner fish that feed on the ectoparasites of fish. We surveyed 969 labrid fishes from the tropical Pacific and found bucephalids only in cleaners (Labroides dimidiatus, L. bicolor, and Bodianus axillaris) and none in piscivores. The prevalences of bucephalids in L. dimidiatus at Lizard Island, Heron Island, Orpheus Island (all on the Great Barrier Reef), New Caledonia, and Moorea (French Polynesia) were 51, 47, 67, 56, and 67%, respectively. All of the L. bicolor examined from Moorea were infected. Bucephalids were highly prevalent in all size classes of L. dimidiatus from Lizard Island. Bucephalids were found in a 1.6-cm long juvenile L. dimidiatus, in which, piscivory is highly unlikely. We examined the literature on the worldwide bucephalid fauna in labrids and all hosts were found to be cleaners (Symphodus tinca, S. mediterraneus, L. dimidiatus, L. bicolor, and Bodianus axillaris) except Notolabrus parilus, whose ecology is unknown. We suggest that cleaners eat bucephalid metacercariae directly from the exterior surface of client fish during cleaning interactions. This is the first evidence of digeneans in the diet of L. dimidiatus, and the first study to show this novel form of parasite transmission where infective stages are eaten as a result of cleaning behaviour. Cleaning-mediated parasite transmission may result in behavioural modification of second intermediate hosts because clients and parasites both benefit from transmission. If the infection is costly to cleaners and acquired during cheating behaviour, then this parasite might regulate mutualism. Alternatively, if infective stages are targeted, infection by these bucephalids may be a negative consequence of an honest foraging strategy.Communicated by: P. F. Sale     

Long-term cleaner fish presence affects growth of a coral reef fish

Cleaning behaviour is considered to be a classical example of mutualism. However, no studies, to our knowledge, have measured the benefits to clients in terms of growth. In the longest experimental study of its kind, over an 8 year period, cleaner fish Labroides dimidiatus were consistently removed from seven patch reefs (61-285 m(2)) and left undisturbed on nine control reefs, and the growth and parasite load of the damselfish Pomacentrus moluccensis determined. After 8 years, growth was reduced and parasitic copepod abundance was higher on fish from removal reefs compared with controls, but only in larger individuals. Behavioural observations revealed that P. moluccensis cleaned by L. dimidiatus were 27 per cent larger than nearby conspecifics. The selective cleaning by L. dimidiatus probably explains why only larger P. moluccensis individuals benefited from cleaning. This is the first demonstration, to our knowledge, that cleaners affect the growth rate of client individuals; a greater size for a given age should result in increased fecundity at a given time. The effect of the removal of so few small fish on the size of another fish species is unprecedented on coral reefs.     

Cleaning interactions at the only atoll in the South Atlantic

In marine ecosystems, cleaning is a mutualistic relationship in which so-called cleaners remove ectoparasites, diseased tissue, or mucus from the body of their clients, and thus help to maintain a healthy reef community. In spite of its importance in many marine habitats, this interaction remains poorly understood, particularly at oceanic islands. Here, we present the first comprehensive study of cleaning interactions in a reef fish assemblage at Rocas, the only atoll in the South Atlantic. We recorded 318 cleaning events, in which six fish species, including two endemic ones, and two shrimp species acted as cleaners. The clients serviced by these cleaners were 21 bony fish species, one shark and one sea turtle. The cleaner wrasse Thalassoma noronhanum and the cleaner goby Elacatinus phthirophagus were the cleaners with the greatest number of events and species richness of clients. Additionally, 82% of clients in the cleaning events were non-piscivores, and the abundance of both cleaners and clients positively influenced the number of cleaning events (R² = 0.4; p < 0.001). Our results indicate that Rocas atoll has a high species richness of cleaner species despite its small size and highlight the importance of studies of cleaning symbiosis, even in isolated places with low species richness, for a better comprehension of this association in reefs.