Cleaner Fish Do Clean!

Summary

'Cleaner fish' are well known to biologists and tourists on the reef. Just what they do though is controversial. Through close observation of the biology of parasites and the cleaning behaviour of client fish, as well as the removal of cleaner fish from small reefs and counts of parasites and fish on these reefs compared to undisturbed reefs, we showed that cleaner fish do indeed have a dramatic effect on the numbers of fish parasites which likely benefit their fish clients. Furthermore, we showed that cleaning behaviour can involve complex cooperative and cognitive behaviours that had generally been assumed to occur only in primates and perhaps only in humans. Finally, we showed that cleaning interactions involve unusual behavioural and colour signals.

Below is a chronology of some of the work we have done involving cleaning behaviour by various cleaner fish and a cleaner shrimp.

Project description

For the past 19 years, we have been studying cleaning behaviours on the Great Barrier Reef. Fish cleaning behaviour involves cleaner fish pecking away at the bodies of fish (clients). Often, clients 'pose' motionless, spreading out their fins to give cleaners access. Some even allow cleaners to enter their mouths and gills - this is especially dramatic when the clients are large predators! Although cleaning interactions are extremely common, until recently there has been much controversy on why client fish seek the services of cleaners and whether parasites motivate this
behaviour.

Fish get cleaned a lot and cleaner fish eat many parasites (gnathiid isopods)

Between 1994 and 1996, we found that a single cleaner fish Labroides dimidiatus inspects more than 2,300 client fish a day from over 130 species and that amazingly, each cleaner fish eats about 1,200 parasites daily. Interestingly, cleaners preferentially eat gnathiid isopod larvae, parasites similar to ticks on land. These, we found, are one of the most common parasites of coral reef fish, but because they are so mobile they had been missed in most previous parasite surveys of fish. By following fish in the field, we determined that most fish are cleaned daily, with individuals of one species (a rabbitfish) seeking cleaners around 144 times a day. This works out to an individual being cleaned every 5 min!

LEFT:Unrolling net to catch fish for parasite load estimates.
RIGHT: Gnathiid ispod. Photo by Peter Parks

Does cleaning affect client parasite loads?

This of course raised the question of whether cleaning then reduces parasite loads on fish. Our early attempts in 1996-1997 to test whether removing cleaner fish from reefs for 6 months affected parasite loads and fish numbers found that these were not affected by cleaner fish presence. However, because in 1998 we had noticed that fish tended to have more gnathiid isopods at dawn than at sunset, we decided to use a different approach to look at this question.

Parasites attack fish day and night

In 1999, we placed fish that normally have relatively high loads of gnathiids in cages on coral reefs. This revealed that fish are attacked by gnathiids at a very rapid rate, but at a higher rate in the late afternoon and at night. Fish are therefore attacked by many of these parasites each day. However, since we had found that gnathiid abundance on wild fish declined between dawn and sunset we wondered whether this decline was due to the actions of cleaners. 

Cleaning dramatically reduces parasite loads over 12 hours!!!

To test this, we placed caged fish on reefs with cleaner fish and on reefs with all cleaner fish removed and found that without cleaners, parasite numbers increased five-fold between dawn and sunset (12 hours!). This suggests that cleaners cause the daily decline of parasites we observed on wild fish. This is the first study to experimentally show that cleaners affect the abundance of parasites on fish and supports the idea that interactions between cleaner fish and clients are mutually beneficial.

 

 

 

 

 

 

PHOTOS: Lexa feeding fish in cages

Parasite infection stimulates client cleaning behaviour

While previous studies suggested that clients sought cleaner fish for the rewarding tactile stimulation the cleaner fish provided (they often gently rub clients with the pelvic fins during cleaning interactions), in 2001 we found that it was parasite infection, not tactile stimulation, which motivated fish to seek cleaner fish. 

PHOTO: Parasitised fish seeking cleaning services from cleaner fish in aquarium.

Cleaner fish engage in complex behaviour

In 2002, in a series of experiments, we showed that cleaning behaviour can be used as a model system to understand the role that partner recognition, partner choice, and partner control play in cooperation among animals. We found that cleaner fish recognize familiar client fish, that clients which had been cheated by cleaners (i.e. bitten) choose to leave such cheaters, and clients which had been cheated controlled their cheating partners by punishing them with vigorous chases. 

PHOTO:Redouan Bshary getting ready
to catch cleaner fish for experiments.

Cleaner fish presence affects client fish abundance and diversity

In 2003, we discovered that cleaner fish affect the abundance and diversity of reef fish. We found that in the absence of cleaner fish (all cleaner fish removed from reefs for 18 months), fish abundance and diversity was one-fourth and one-half, respectively, compared to that on reefs with cleaner fish. But only mobile fishes were affected with resident fishes not affected at all. Thus many fish appear to choose reefs based on the presence of cleaner fish and may leave if there are no cleaner fish.

LEFT: Lagoon site showing experimental reefs (small reefs along bottom)
RIGHT: Casuarina Beach site showing experimental reefs (circle of small reefs in centre)

Parasitic gnathiid isopods feeding rates explain frequent client cleaning

A surprising finding that same year was that gnathiids fill up on fish blood very rapidly and only remain on fish for less than an hour. These, combined with other findings that they infect fish 24 hours a day, may explain why client fish seek cleaner repeatedly and at such short intervals. By going to cleaners often, it is more likely that the client's gnathiids will be removed, and that this will occur before gnathiids remove too much blood from the client.

Cleaner fish prefer fish mucus over gnathiid ispods

A discovery in 2004 that changed the way we viewed cleaning behaviour was the finding that, when given a choice of gnathiids or mucus (offered on plates), trained cleaner fish surprisingly preferred the mucus. Since mucus provides valuable benefits to the client, this suggested that such a preference by the cleaner was in conflict with the client's needs, and supports observations emphasizing the importance of partner control in keeping cleaning interactions mutualistic. Another study showed they preferred parrotfish over snapper mucus, suggesting the degree of conflict between cleaners and clients may vary among client species.

LEFT: Cleaner fish choosing mucus over gnathiids.
RIGHT: Cleaner fish choosing parrotfish mucus over snapper mucus.

Tactile stimulation while dancing prevents conflicts with predators

In cleaning interactions, the classical question asked is why cleaner fish can clean piscivorous client-fish without being eaten. In 2004, we showed 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 pre-conflict management strategy that enables cleaner fish to avoid conflict with potentially ‘dangerous' clients. How cleaner fish can tell a client is hungry, however, remains a mystery.

PHOTO:Fabian cleaning piscivorous fish holding tanks.

Rocking dance in cleaner advertises cleaning services

The following year, we found that a “rocking dance” is used by cleaner shrimp to advertise cleaning services. Shrimp “rock dance” when approaching potential client fish and do so more when they are hungry. When given a choice, clients preferred hungry, rocking shrimp. The rocking dance therefore influenced client behaviour and thus appears to function as a signal to advertise the presence of cleaner shrimp to potential clients.

LEFT: Rock dancing cleaner shrimp.
RIGHT: Justine observing cleaner shrimp and client fish.

Client chasing makes cleaner fish behave

Cleaner fish sometimes cheat and eat client mucus or skin. Field observations suggest that clients control such cheating by using punishment (chasing the cleaner) or by switching partners (fleeing from the cleaner). Therefore, in 2005, we tested experimentally whether such client behaviours result in cooperative cleaner fish. Cleaners were allowed to feed from 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, this suggested that the same behaviours in clients improve the service quality of cleaners under natural conditions.

Eavesdropping pays off in cleaning interactions

In 2006, we found the first experimental evidence for ‘simple' indirect reciprocity in animals. We found that eavesdropping clients spent more time next to ‘cooperative' compared with ‘non-cooperative' cleaners which shows clients engage in image scoring behaviour. Furthermore, trained cleaners learned to feed against their preference – which corresponds to cooperatively eating ectoparasites rather than uncooperatively eating client mucus in the wild - in an ‘image scoring' context.

Gnathiid isopods implicated as vectors of blood parasites

That same year, we also found that some coral reef fish have blood parasites (haemogregarines), and that gnathiid isopods pick up these infections when feeding on the blood of these fishes. This suggested gnathiids might transmit these infections between fishes, much like mosquitoes transmit malaria. This is currently being examined Lynda Curtis.

LEFT: Blood parasites from a triggerfish.
RIGHT: Lynda, Ange, Rachel, Lexa, Conor, and Nico working on isopods.

More clients means more cleaning

In 2007, using a meta-analysis of client-cleaner interactions involving 11 cleaner organisms from Brazil, the Caribbean, the Mediterranean and Australia, we found that there was a strong, positive effect of client abundance on cleaning frequency, but only a weak, negative effect of client body size. These effects were modulated by client trophic group and social behaviour. This study adds to a growing body of evidence suggesting a central role of species abundance in structuring species interactions.

Cleaner fish have super sunscreens

Coral reef fishes were recently discovered to have ultraviolet radiation (UV) screening compounds, most commonly known as mycosporine-like amino acids (MAAs), in their external body mucus. However, little is known about the identity and quantity of MAAs in the mucus of reef fish or what factors affect their abundance and distribution. Therefore, in 2008, we examined these using 7 coral fishes, including the cleaner fish Labroides dimidiatus. MAAs were found in the mucus of all the fishes. Interestingly, in comparison to most of the other species, cleaner fish had a relatively high concentration of all MAAs. Since fishes cannot produce their own MAAs but must obtain them via their diet, it raised the question of the source of MAAs in L. dimidiatus. This is currently being examined.

PHOTO: Maxi doing cleaner fish sunscreen experiments.

Cleaning stations are safe havens

Cleaner fish are thought to benefit from immunity to predation and use tactile stimulation as a pre-conflict management strategy to manipulate partners' decisions and to avoid being eaten by piscivorous client fish. In 2008, we showed that the presence of cleaner fish resulted in nearby fish not involved in the cleaner–client mutualism experiencing less aggression (chases) from predatory clients. In addition, the rate that predatory clients chased prey was negatively correlated with the amount of tactile stimulation given to the predator by the cleaner. These data suggest that, in the laboratory, the risk of aggression from predators toward nearby prey fish was greatly reduced as a by-product of cleaner fish presence and tactile stimulation of predators by cleaner fish. These results raise the question of whether cleaning stations act as safe havens from predator aggression.

PHOTO: Karen Cheney observing cleaning behaviour in tubs.

Cleaner fish mimics can change their colours

Facultative mimicry, the ability to switch between mimic and non-mimic colours at will, is uncommon in the animal kingdom, but has been shown in a cephalopod, and recently by us in a marine fish, the bluestriped fangblenny Plagiotremus rhinorhynchos, an aggressive mimic of the juvenile cleaner fish Labroides dimidiatus. In 2008, we demonstrated for the first time that fangblennies adopted mimic colours in the presence of juvenile cleaner fish; however, this only occurred in smaller individuals. Field data indicated that when juvenile cleaner fish were abundant, the proportion of mimic to non-mimic fangblennies was greater, suggesting that fangblennies adopt their mimic disguise depending on the availability of cleaner fish.

Couples are better cleaners

In 2008, we presented a game-theory model based on the marginal value theorem, which predicted that as long as the client determines the duration, and the providers cooperate towards mutual gain, service quality will increase in the pair situation. This was demonstrated using cleaning mutualism, in which stable male–female pairs of the cleaner fish Labroides dimidiatus repeatedly inspect client fish jointly. Because clients often leave in response to cleaner fish cheating (feeding on mucus), the benefits of cheating can be gained by only one cleaner during a pair inspection. We found increased service quality during pair inspections. This was mainly due to the smaller females behaving significantly more cooperatively than their larger male partners.

A ton of gnathiids are gobbled up daily

In 2008, we examined the large scale interactions between gnathiid isopods, cleaner fish, and other fish. We calculated that the abundance of gnathiids emerging from the reef in search of hosts (gnathiids only are on fish while sucking fish blood, returning to the reef to digest and moult to the next stage) was 42 per metre squared per day or 4552 per reef (approximately 100 metres squared area) per day. This works out to about 5 emerging gnathiids per fish, but excluding the rarely infested pomacentrid fishes, this works out to 21 gnathiids per fish per day. Overall, the abundance of emerging gnathiids per patch reef was 66% of the number of gnathiids that all adult cleaner fish per reef eat daily while engaged in cleaning behaviour. That L. dimidiatus eat more gnathiids per reef daily than were sampled with emergence traps suggests that cleaner fish are an important source of mortality for gnathiids.

PHOTO: Lexa collecting gnathiids using an emergence trap.

Cleaner fish standout on the reef and tend to be blue

A common question in cleaning behaviour is how clients recognize cleaners and decide not to eat them. A longheld belief is that cleaner fish display a blue ‘‘guild'' coloration. In 2009, via color analytical techniques and phylogenetic comparisons, we showed that cleaner fish are more likely to display a blue coloration, in addition to a yellow coloration, compared to noncleaner fish. Via theoretical vision models, we show that, from the perspective of potential signal receivers, blue is the most spectrally contrasting colour against coral reef backgrounds, whereas yellow is most contrasting against blue water backgrounds or against black lateral stripes. Finally, behavioural experiments confirmed that blue within the cleaner fish pattern attracted more client reef fish to cleaning stations. Cleaner fish thus have evolved some of the most conspicuous combinations of colours and patterns in the marine environment, and this is likely to underpin the success of the cleaner-client relationship on the reef.

Punishment promotes cooperation

Why do humans punish others even if they themselves are not the victim? Such behaviour has long been interpreted as one that benefits the group and not the individual that is doing the actual punishing. But theory predicts it can also benefit the individual. To test this, in 2010 we offered cleaner fish preferred and non preferred food (fish flakes) on a plate. If the female cheated and ate the preferred food (prawn) we removed the plate immediately. The male then chased the female as punishment for her cheating behaviour. After a number of punishments, the female became more cooperative and would then continue to eat from the non-preferred plate allowing the male to obtain more food. Thus punishment meted out by male cleaner fish toward female cleaner fish promoted cooperation and as a result rewarded the male with more food because it assured the client did not leave the cleaning station. This showed that understanding the behaviour of self-interested cleaner fish in response to personal loss may be a key step toward understanding why humans find it necessary to punish a third-party when they receive no direct benefit.

 

All the above information is published. Please see publications list for more details.

 

PHOTO: The Coral Reef Ecology Lab on Lizard Island, summer of 2005.

 

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