What is a cleaner fish? When snorkelling, you might have seen a fish acting strangely, possibly hovering with its mouth open and fins spread out. If you were lucky, you might have seen another smaller fish probing around its fins, gills, mouth, and body. This is known as cleaning behaviour and involves ‘cleaners’, animals which remove parasites, tissue, mucus and sometimes even blood from other animals referred to as hosts, customers or clients. Cleaners include polychaetes, crustaceans, ants, lizards, turtles, and most commonly, birds and fishes. While birds are well-known for cleaning crocodiles and mammals, cleaner fish generally clean other fishes, including sharks and rays, but some also clean lobsters, turtles, octopuses, marine iguanas, whales, and even hippopotamuses.

Which fish clean? Cleaning behaviour in fishes has evolved independently a number of times in a variety of different fish lineages. Cleaner fish are found in marine, freshwater and brackish water all over the world. Marine cleaner fish include many wrasses, and some triggerfish, butterflyfish, diskfish, damselfish, angelfish, gobies, leatherjackets, pipefish, seachubs, surfperch, suckerfish, jacks and topsmelt. Freshwater cleaner fishes include cichlids, guppies, carp, centrarchids, killifish and sticklebacks.

Why are cleaner fish important or of interest? Because cleaner fish eat presumably harmful ectoparasites, and because they clean damaged tissue in wounds of fish, it is generally assumed that their services improve the health of their clients. The ecological significance of most cleaner fishes has not been studied, exceptions being the Indo-Pacific blue-streaked cleaner wrasse Labroides dimidiatus ( Figure 1 Cleaner fish Labroides dimidiatus cleaning a client Zebrasoma veliferum. Photo by Karen Cheney. Because cleaner fish eat presumably harmful ectoparasites, and because they clean damaged tissue in wounds of fish, it is generally assumed that their services improve the health of their clients. The ecological significance of most cleaner fishes has not been studied, exceptions being the Indo-Pacific blue-streaked cleaner wrasse Labroides dimidiatus ( Figure 1 ), Caribbean Elacatinus spp. gobies, and wrasses used in the biological control of sea lice infecting farmed salmon.

Of all cleaner species, L. dimidiatus is the best studied. Each cleaner fish eats about 1200 parasites a day, most of which are gnathiid isopods, and inspects about 2300 fish a day. In their absence, gnathiids on caged fish increase four-fold over the course of 12 hours; in very large numbers, they can kill fish. Interestingly, gnathiids have been implicated as vectors of blood parasites, such as haemogregarines, but whether cleaner fish control these fish diseases remains unknown. The presence of L. dimidiatus has been associated with a reduction in a client's stress response, measured with cortisol levels. L. dimidiatus also affects the behaviour and distribution of fish. Gnathiid infection stimulates fish to seek L. dimidiatus, with larger clients seeking cleaning more frequently than smaller ones. For example, individual rabbitfish seek a L. dimidiatus about 144 times a day or every five minutes. One explanation for this high visitation rate and short interval between visits is that gnathiids constantly attack fish and feed rapidly. By getting cleaned repeatedly, clients potentially increase the likelihood that their gnathiids are removed before they have ingested much blood. L. dimidiatus also affect the local diversity of coral reef fishes. When they were removed from small reefs, the diversity of fish decreased dramatically; adding cleaner fish made diversity go up. The fish species involved include large herbivores or roving carnivores, which themselves can directly and indirectly affect the benthic community structure.

Can cleaner fish help us better understand ourselves? Surprisingly, yes. How cooperation among animals, including humans, evolved and how it is maintained when cheating is often theoretically more profitable has long fascinated scientists and the general public. While cleaner fish can cooperate and eat ectoparasites, they can also cheat on their clients by eating client material, such as mucus. Indeed, L. dimidiatus prefer client mucus yet they mostly eat the less-preferred gnathiid isopods and thus they tend to feed against their preference (that is, cooperate or not cheat). Some clients can also cheat by eating the cleaner fish. Thus, how clients control cheating cleaners, and vice versa, provides insight into the mechanisms involved in maintaining cooperation. An easy way to test many general hypotheses about cooperation is to use the food preferences of L. dimidiatus to simulate cheating or cooperative behaviour and to manipulate the behaviour of model clients (plates with food on them). Cleaners are trained to feed off plates containing two food types: preferred prawn and less-preferred fish flake. Eating prawn corresponds to cheating the client by eating mucus, whereas eating flake corresponds to cooperating by removing ectoparasites. Eating prawn results in the immediate removal of the plate.

For example, it is well known that humans punish cheaters even if this punishment is costly. Such behaviour has long been interpreted as one that benefits the group and not the individual, despite theoretical predictions that third-party punishment can yield individual benefits to the punisher. When cleaning in male–female pairs, the male cleaner fish punishes the cheating female by chasing her, even though he is not the primary victim. Such cheating results in the loss of the client to both partners. In the laboratory, this punishment promotes female cooperation (feeding on flakes), yielding direct foraging benefits to the male (more total food items off the plates). This showed that ‘third-party’ punishment can evolve via self-serving, rather than altruistic, tendencies which may be a key step toward third-party punishment by non-victims as seen in humans.

Cleaner fish have also provided insight into why humans often help unrelated individuals that may never reciprocate the altruist's favour. Such behaviour has been explained by the altruist's gain in social image: image-scoring bystanders, also known as eavesdroppers, notice the altruistic act and therefore are more likely to help the altruist in the future. Such complex indirect reciprocity based on altruistic acts may evolve only after simple indirect reciprocity has been established. Experimental evidence for both of the requirements of simple indirect reciprocity were shown using L. dimidiatus. Other abilities of cleaner fish to deal with complex social environments in this cleaning mutualism include individual recognition, interspecific signaling to manage conflicts, manipulating partners, reconciling, and using altruism, abilities that are also the focus of cognitive studies of primates.

Do all cleaner fish behave the same way? Certainly not. There are obligate cleaner fish, mainly Labroides spp. wrasses and Elacatinus spp. gobies, which obtain most of their food via cleaning. Some obligate cleaners, such as L. bicolor and L. phthirophagus, mostly eat fish mucus and so are not considered as cooperative as the rest. But even the supposedly very cooperative ones, like L. dimidiatus, will eat mucus when they can get it. Most cleaner fish, however, are facultative cleaners which means they do not rely solely on cleaning for food. Facultative cleaners tend to be juveniles, such as some butterfly and angel fishes and many wrasses. Some wrasse clean fish as juveniles but eat corals as adults.

What are the latest findings on cleaner fish? The evolutionary stability of cleaning mutualism has been recently examined. Cleaning interactions resemble the Prisoner's Dilemma: predators can cheat by eating the cleaner, while cleaners can cheat by eating mucus; hence both partners may cooperate or defect. But the solution is not a form of reciprocity, because the predator terminates the game if it cheats and so tit-for-tat-like strategies are not possible. Hence, L. dimidiatus are virtually unconditionally cooperative towards predators in the wild, though less so in the laboratory. L. dimidiatus also provide much tactile stimulation (rubbing with their pelvic fins) to predators, apparently to reduce conflicts from occurring. Non-predatory clients, however, use different control mechanisms: clients that can access only one cleaning station rely on aggression to control cheating cleaners, whereas those that can access more than one station flee and switch to another station. Oddly, the risk of aggression from predators toward nearby prey fish is greatly reduced as a by-product of cleaner fish presence and the tactile stimulation of predators by cleaner fish, suggesting cleaning stations act as safe havens from predator aggression.

Probably no surprise to most snorkelers, a recent study confirmed that cleaner fish have evolved some of the most conspicuous combinations of colors and patterns in the marine environment: they tend to be yellow or blue, aspects that are in stark contrast to their stripes and make them stand out from the reef background; blue in cleaners also attracts more clients to cleaning stations. Many new species of cleaner fishes have also been reported, even one of a shark apparently functioning as a ‘cleaner’ with a ‘client’ fish scraping its body against the shark's body; in this case there appears to be no benefit to the cleaner. Intriguingly, a recent molecular analysis suggests that cleaning in Labroides spp. evolved once, from a coral feeding lineage in the Miocene (∼9.5 million years ago).

Any other oddities about cleaner fish? You bet! L. dimiditus become infected as a result of their cleaning behaviour when they feed on parasitic worms encysted in the skin of clients, a novel form of parasite transmission mediated by cleaning. And remarkably, L. dimidiatus cleans its mimic, the fangblenny Aspidontus taeniatus.

Should we keep cleaner fish in aquaria? Probably not. Surprisingly, L. dimidiatus are one of the top ten most exported fish to the US and UK. In Sri Lanka alone, an astonishing 20,000 were traded one year. The direct and indirect effects of the large-scale removal of this ecologically important species are unknown. To make matters worse, aquarium suitability information indicates L. dimidiatus is one of the two top species known not to acclimatize well to aquarium conditions. The other is mandarin fish. In Brazil, cleaner gobies were the sixth most exported marine ornamental fish species between 1999 and 2001. Unfortunately, only some cleaner gobies and temperate cleaner wrasse are bred in captivity.

Who cleans the cleaners? Everyone asks this question. They clean each other! Especially L. dimidiatus. Guppies in aquaria do too and you don't need to go snorkelling to see that!

Where can I find out more about cleaner fish? Bshary R.

Côté I.M. New perspectives on marine cleaning mutualism. in: Magnhagen C. Braithwaite V.A. Forsgren E. Kapoor B.G. Fish Behaviour. Science Publishers , Enfield NH : 563-592 Crossref

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