Client Reef Fish Research Articles

The cleaning goby mutualism: a system without punishment, partner switching or tactile stimulation

AbstractIn the cleanerfish–client mutualism involving the Indo‐Pacific cleaner wrasse Labroides dimidiatus and its reef fish clients, mechanisms such as ‘tactile stimulation’, partner switching and punishment are used by clients to control cheating by cleaners. We sought to establish whether these behaviours are general features of cleaning mutualisms by examining their presence in interactions between Caribbean cleaning gobies (Elacatinus spp.) and their clients. The cleaning goby–client mutualism bears several similarities to the cleaner wrasse system: clients visit cleaners frequently to have their ectoparasites removed while cleaners depend heavily on these visits for food, and cheating by cleaning gobies is also prevalent. However, our data revealed striking differences between the two cleanerfish systems: clients did not seem to attempt to control cheating by cleaning gobies and cleaning gobies did not perform tactile stimulation on their clients. We suggest three hypotheses that might explain these major differences between both systems, based on differences in mutual dependence between cleaners and clients or cognitive ability of cleaners, differences in costs of being cheated and differences in foraging preferences by cleaners. Interactions between L. dimidiatus and its clients should probably not be seen as the ‘standard’ marine fish cleaning mutualism.

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

BackgroundMarine 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.ResultsFor 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.ConclusionIt 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.

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.

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.

Building up relationships in asymmetric co-operation games between the cleaner wrasse Labroides dimidiatus and client reef fish

It has been suggested that individuals may prevent partners from cheating by building up relationships slowly, giving very little in the beginning and raising the stakes in subsequent moves if partners reciprocate. I tested this idea with field experiments on the cleaner-fish Labroides dimidiatus and its reef fish. Clients visit cleaners at their small territories, so-called cleaning stations, to have parasites removed. Cleaners were first observed and then caught and either put back on their original territory or moved to a new site. I noted a variety of cleaner and client behaviour to evaluate how, if at all, relationships are built up. Cleaners and resident clients indeed build up relationships, but with heavy initial investment. There was no evidence that cleaners build up relationships with client species that have access to several cleaners. Finally, it appeared that cleaners constantly invest in relationships with predatory clients, possibly to reduce the risk that predators try to catch them. I propose that asymmetries between partners with respect to either payoff values or strategic options are the major reason why the results do not fit the so-called raising-the-stakes strategy.

Cleaner fish Labroides dimidiatus recognise familiar clients.

Individual recognition has been attributed a crucial role in the evolution of complex social systems such as helping behaviour and cooperation. A classical example for interspecific cooperation is the mutualism between the cleaner fish Labroides dimidiatus and its client reef fish species. For stable cooperation to evolve, it is generally assumed that partners interact repeatedly and remember each other's past behaviour. Repeated interactions may be achieved by site fidelity or individual recognition. However, as some cleaner fish have more than 2,300 interactions per day with various individuals per species and various species of clients, basic assumptions of cooperation theory might be violated in this mutualism. We tested the cleaner L. dimidiatus and its herbivorous client, the surgeon fish Ctenochaetus striatus, for their ability to distinguish between a familiar and an unfamiliar partner in a choice experiment. Under natural conditions, cleaners and clients have to build up their relationship, which is probably costly for both. We therefore predicted that both clients and cleaners should prefer the familiar partner in our choice experiment. We found that cleaners spent significantly more time near the familiar than the unfamiliar clients in the first 2 minutes of the experiment. This indicates the ability for individual recognition in cleaners. In contrast, the client C. striatus showed no significant preference. This could be due to a sampling artefact, possibly due to a lack of sufficient motivation. Alternatively, clients may not need to recognise their cleaners but instead remember the defined territories of L. dimidiatus to achieve repeated interactions with the same individual.

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.

Parasite distribution on client reef fish determines cleaner fish foraging patterns

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 235:217-222 (2002) - doi:10.3354/meps235217 Parasite distribution on client reef fish determines cleaner fish foraging patterns Redouan Bshary1,2,*, Alexandra S. Grutter3 1Max-Planck-Institut für Verhaltensphysiologie, Seewiesen, Postfach 1564, 82305 Starnberg, Germany 2University of Cambridge, Department of Zoology, Downing Street, Cambridge CB2 3EJ, United Kingdom 3Department of Zoology and Entomology, The University of Queensland, Brisbane, Queensland 4072, Australia *Address for correspondence: University of Cambridge, Department of Zoology, Downing Street, Cambridge CB2 3EJ, United Kingdom. E-mail: rb286@cam.ac.uk ABSTRACT: Recent evidence suggests that cleaner fish Labroides dimidiatus effectively control parasite densities on client reef fish that actively visit them to have parasites and dead or infected tissue removed. These findings support the hypothesis that clients benefit from cleaning. However, they do not show how cleaners reduce the parasite load of their clients. Cleaners could selectively feed on parasites or parasite removal could be a side product of cleaners foraging indifferently on the client surface, resulting in the removal of healthy mucus and scales also. To investigate cleaner fish foraging behaviour, we infected individuals of the surgeon fish Ctenochaetus striatus, with parasitic monogeneans on one body side, while the other body side was parasite free. We then allowed these clients to interact with L. dimidiatus. We found that the duration of interactions depended on parasite load, and that cleaners spent both more time and took more bites per time unit on the infected than on the uninfected side. Our data thus support the idea that parasite abundance determines food patch quality for cleaners. The overall outcome of cleaning interactions is thus likely to benefit the clients. KEY WORDS: Cleaning behaviour · Cooperation · Mutualism · Selective foraging · Labroides dimidiatus Full text in pdf format PreviousNextExport citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 235. Online publication date: June 19, 2002 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2002 Inter-Research.