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.

     

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.     

Cleaning up the biogeography of Labroides dimidiatus using phylogenetics and morphometrics

Cleaner fishes are some of the most conspicuous organisms on coral reefs due to their behaviour and prominent body pattern, consisting of a lateral stripe and blue/yellow colouration. All obligate cleaner fishes share this body stripe pattern, which is an important signal for attracting client fishes. However, variability in the cleaning signal of the cleaner fish Labroides dimidiatus has been documented across its range. Here, we investigate the geographic distribution of cleaner signal polymorphisms in L. dimidiatus and contrast this to phylogeographic variation in mitochondrial (mt) DNA. We used samples from 12 sites for genetic analyses, encompassing much of L. dimidiatus’ range from the Red Sea to Fiji. We obtained morphometric measures of the cleaner signal body stripe width from individuals among six of the sites and qualitatively grouped tail stripe shape. mtDNA control region sequences were used for phylogenetic and population genetic analyses. We found that body stripe width was significantly correlated with tail stripe shape and geographical location, with Indian Ocean populations differing in morphology from western Pacific populations. L. dimidiatus haplotypes formed two reciprocally monophyletic clades, although in contrast to morphology, Japanese cleaner fish fell within the same clade as Indian Ocean cleaner fish and both clade types were sympatric in Papua New Guinea. An additional novel finding of our research was that the inclusion of two closely related cleaner fish species, Labroides pectoralis and Labroides bicolor, in the phylogenetic analysis rendered L. dimidiatus polyphyletic. Overall, the findings suggest the diversity within L. dimidiatus is underestimated.     

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.     

Multiple cleaner species provide simultaneous services to coral reef fish clients

Cleaning symbioses on tropical coral reefs are typically documented between two species: a single client fish and one or more conspecific cleaners. However, multiple cleaner species living sympatrically in the Caribbean have been anecdotally reported to simultaneously clean the same client. Nothing is known about the patterns and processes driving these interactions, which may differ from those involving a single cleaner species. Here, we used remote underwater videography on three reefs in Honduras to record simultaneous cleaning interactions involving Pederson''s cleaner shrimp (Ancylomenes pedersoni) and cleaner gobies (Elacatinus spp.). A pilot study on adjacent shrimp and goby stations found interactions were always initiated by shrimp. A larger, multi-year dataset shows cleaner gobies joined 28% of all interactions initiated at A. pedersoni cleaning stations with cleaner gobies residing nearby. Client body size significantly predicted simultaneous cleaning interactions, with 45% of interactions simultaneous for clients greater than 20 cm total body length compared with only 8% for clients less than 20 cm. We also found that simultaneous cleaning interactions lasted over twice as long as shrimp-only interactions. We propose these novel multi-species interactions to be an ideal model system to explore broader questions about coexistence, niche overlap and functional redundancy among sympatric cleaner species.     

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 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.     

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.     

Crime and punishment in a roaming cleanerfish

Cheating is common in cooperative interactions, but its occurrence can be controlled by various means ranging from rewarding cooperators to active punishment of cheaters. Punishment occurs in the mutualism involving the cleanerfish Labroides dimidiatus and its reef fish clients. When L. dimidiatus cheats, by taking scales and mucus rather than ectoparasites, wronged clients either chase or withhold further visits to the dishonest cleaner, which leads to more cooperative future interactions. Punishment of cheating L. dimidiatus may be effective largely because these cleaners are strictly site-attached, increasing the potential for repeated interactions between individual cleaners and clients. Here, we contrast the patterns of cheating and punishment in L. dimidiatus with its close relative, the less site-attached Labroides bicolor. Overall, L. bicolor had larger home ranges, cheated more often and, contrary to our prediction, were punished by cheated clients as frequently as, and not less often than, L. dimidiatus. However, adult L. bicolor, which had the largest home ranges, did not cheat more than younger conspecifics, suggesting that roaming, and hence the frequency of repeated interactions, has little influence on cheating and retaliation in cleaner–client relationships. We suggest that roaming cleaners offer the only option available to many site-attached reef fish seeking a cleaning service. This asymmetry in scope for partner choice encourages dishonesty by the partner with more options (i.e. L. bicolor), but to be cleaned by a cleaner that sometimes cheats may be a better option than not to be cleaned at all.     

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 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.     

Does client size affect cleaner fish choice of client? An empirical test using client fish models

To determine whether the choice of client fishes in the cleaner fish Labroides dimidiatus was influenced by client size, cleaner fish were given a choice of equal amount of food spread on large and small client redfin butterflyfish Chaetodon trifasciatus models. All large models received bites from cleaners compared to 27% for small models. Seventy‐nine per cent of cleaners took their first bite from the large fish model. The results suggest that client size may affect cleaner fish choice.     

Do cleaning organisms reduce the stress response of client reef fish?

Background

Marine cleaning interactions in which cleaner fish or shrimps remove parasites from visiting 'client' reef fish are a textbook example of mutualism. However, there is yet no conclusive evidence that cleaning organisms significantly improve the health of their clients. We tested the stress response of wild caught individuals of two client species, Chromis dimidiata and Pseudanthias squamipinnis, that had either access to a cleaner wrasse Labroides dimidiatus, or to cleaner shrimps Stenopus hispidus and Periclimenes longicarpus, or no access to cleaning organisms.

Results

For both client species, we found an association between the presence of cleaner organisms and a reduction in the short term stress response of client fish to capture, transport and one hour confinement in small aquaria, as measured with cortisol levels.

Conclusion

It is conceivable that individuals who are more easily stressed than others pay a fitness cost in the long run. Thus, our data suggest that marine cleaning mutualisms are indeed mutualistic. More generally, measures of stress responses or basal levels may provide a useful tool to assess the impact of interspecific interactions on the partner species.     

Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish.

Cleaning behaviour is a popular example of non-kin cooperation. However, quantitative support for this is generally sparse and the alternative, that cleaners are parasitic, has also been proposed. Although the behaviour involves some of the most complex and highly developed interspecific communication signals known, the proximate causal factors for why clients seek cleaners are controversial. However, this information is essential to understanding the evolution of cleaning. I tested whether clients seek cleaners in response to parasite infection or whether clients seek cleaners for tactile stimulation regardless of parasite load. Parasite loads on client fish were manipulated and clients exposed to cleaner fish and control fish behind glass. I found that parasitized client fish spent more time than unparasitized fish next to a cleaner fish. In addition, parasitized clients spent more time next to cleaners than next to control fish, whereas unparasitized fish were not attracted to cleaners. This study shows, I believe for the first time, which is somewhat surprising, that parasite infection alone causes clients to seek cleaning by cleaners and provides insight into how this behaviour evolved.     

Cleaning behaviour of the cichlid Mesonauta festivus in the Pantanal wetlands: evidence of a potential freshwater cleaning station

Cleaning interactions are known among several groups of fishes, with a higher number of records for marine fish species. These temporary associations occur between one species that acts as the cleaner and the other species as the client. The interaction usually takes place within the boundaries defined by the cleaner. This site, known as the cleaning station, allows the client fish to strike a typical pose allowing the cleaner to approach, such as wide-open fins and inclined, motionless body. Few studies have reported on the cleaning behaviour of freshwater fish species, and none has reported on behaviour that could be interpreted as establishing a cleaning station. Herein we present a new record of the cleaning interaction in the Neotropics, between the cichlid Mesonauta festivus as the cleaner and three species of anostomid (Leporinus macrocephalus, Leporinus friderici and Schizodon borellii) as clients on Pantanal wetlands, as well as the establishment of a defined cleaning station.     

Effects of group behavior in the predatory raid on damselfish nests by the false cleanerfish Aspidontus taeniatus

The false cleanerfish Aspidontus taeniatus, which resembles the bluestreak cleaner wrasse Labroides dimidiatus, is one of the best-known examples of mimicry in vertebrates. This mimicry system has been viewed as an aggressive mimicry to bite fish fins. However, recent field studies have reported that large individuals of the false cleanerfish often form groups and jointly raid damselfish nests to eat eggs that are guarded by their parents. The benefits of group behavior have been reported in a variety of animals. In the case of false cleanerfish, parental defense of territorial damselfishes is the main factor that constrains the availability of nutritionally valuable food resources. Here, we conducted field observations on the reefs of Okinawa, and found that the false cleanerfish formed groups of 2–12 individuals when they raided breeding nests of 13 species of damselfishes (Pomacentridae) and one species of triggerfish (Balistidae). Since the cleaner wrasse does not form such groups, the feeding groups of the false cleanerfish are assumed to reduce the effectiveness of mimicry. However, our results showed that the group behavior has two effects: a dilution effect, which reduces the risk of being attacked by egg-guarding fish, and an increase in foraging efficiency. We conclude that the false cleanerfish need to form foraging groups during egg-eating because the mimicry has no effect on parental damselfishes.     

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.     

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 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.