Alexandra S. Grutter

Image scoring and cooperation in a cleaner fish mutualism

Humans are highly social animals and often help unrelated individuals that may never reciprocate the altruists favour. This apparent evolutionary puzzle may be explained by the altruists 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, which requires two steps. First, image scoring evolves when bystanders gain personal benefits from information gathered, for example, by finding cooperative partners. Second, altruistic behaviour in the presence of such bystanders may evolve if altruists benefit from access to the bystanders. Here, we provide experimental evidence for both of the requirements in a cleaning mutualism involving the cleaner fish Labroides dimidiatus. These cleaners may cooperate and remove ectoparasites from clients or they may cheat by feeding on client mucus. As mucus may be preferred over typical client ectoparasites, clients must make cleaners feed against their preference to obtain a cooperative service. We found that eavesdropping clients spent more time next to ‘cooperative’ than ‘unknown cooperative level’ cleaners, which shows that clients engage in image-scoring behaviour. Furthermore, trained cleaners learned to feed more cooperatively when in an ‘image-scoring’ than in a ‘non-image-scoring’ situation.

Cleaner fish really do clean

The cleaning of client fish by cleaner fish is one of the most highly developed interspecific communication systems known. But even though it is a seemingly obvious mutualism, several quantitative studies have failed to show any benefit for the clients, leading to the hypothesis that cleaner fish are ‘behavioural parasites’ that exploit the sensory system of the clients to obtain food, rather than to increase the clients fitness. The cleaner fish Labroides dimidiatus eats parasitic gnathiid isopods, which decline in number on the client fish Hemigymnus melapterus daily between dawn and sunset. I find that the cleaner fish reduces parasite abundance, resulting in a 4.5-fold difference within 12 hours, supporting the hypothesis that cleaning behaviour is mutualistic.

Punishment and partner switching cause cooperative behaviour in a cleaning mutualism

Abstract: 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.

Spatiotemporal Variation and Feeding Selectivity in the Diet of the Cleaner Fish Labroides dimidiatus

The composition of the diet of the cleaner wrasse Labroides dimidiatus was quantified at different times and at tao spatial scales. I examined feeding selectivity in the cleaner fish by comparing its diet to the parasite: load of seven species of fish hosts it regularly cleans. Parasitic gnathiid isopods made up 50% of the estimated food volume and 95% of the prey items of Labroides dimidiatus at Lizard Island, Australia. The remaining 50% of the food material mainly was unidentified digested organic matter. Tnf greatest difference in the diet occurred between Heron and Lizard Islands, with only small differences among sites at the latter The total biomass of gnathiid isopods in the diet was four times higher at Lizard Island than at Heron Island, Fish from Lizard Island contained more caligid larvae and other parasitic copepods in their diet, whereas fish from Heron Island contained more nonparasitic copepods and mucus. The number and estimated biomass of gnathiids in the diet more than doubled from May to January. Variation in the diet implies spatial and temporal flexibility in the foraging patterns of L. dimidiatus. The higher ratio of gnathiids to other crustacea in the diet compared to that on host fish, suggests that L. dimidiatus is a selective feeder.

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.

Pairs of cooperating cleaner fish provide better service quality than singletons

Service providers may vary service quality depending on whether they work alone or provide the service simultaneously with a partner. The latter case resembles a prisoner’s dilemma, in which one provider may try to reap the benefits of the interaction without providing the service. Here we present a game-theory model based on the marginal value theorem, which predicts 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 prediction is consistent with field observations and with an experiment on cleaning mutualism, in which stable male–female pairs of the cleaner wrasse Labroides dimidiatus repeatedly inspect client fish jointly. Cleaners cooperate by eating ectoparasites off clients but actually prefer to cheat and eat client mucus. Because clients often leave in response to such cheating, the benefits of cheating can be gained by only one cleaner during a pair inspection. In both data sets, the increased service quality during pair inspection was mainly due to the smaller females behaving significantly more cooperatively than their larger male partners. In contrast, during solitary inspections, cleaning behaviour was very similar between the sexes. Our study highlights the importance of incorporating interactions between service providers to make more quantitative predictions about cooperation between species.

Punishers Benefit From Third-Party Punishment in Fish

In cleaner fish, punishment of foraging partners who cheat a client benefits punishers by increasing future cooperation. In cases where uninvolved bystanders pay to punish defectors, this behavior has typically been interpreted in terms of group-level rather than individual-level benefits. Male cleaner fish, Labroides dimidiatus, punish their female partner if she cheats while inspecting model clients. Punishment promotes female cooperation and thereby yields direct foraging benefits to the male. Thus, third-party punishment can evolve via self-serving tendencies in a nonhuman species, and this finding may shed light on the evolutionary dynamics of more complex behavior in other animal species, including humans.

Cleaning symbioses: Proximate and adaptive explanations

which proceeds to remove ectoparasitic worms and crustaceans from the larger fish. On the African savanna, a bird lands on the back of a grazing zebra, and while the zebra stands still the bird patrols the zebras body, searching out and eating ticks and other ectoparasites. These are two examples of cleaning symbioses-one of the most remarkable classes of ecological interactions between taxonomically unrelated organisms. Over the past few decades, as reflected in the above excerpts, the opinion of scientists regarding cleaning symbioses has changed, from selfless cooperation, to a mutually beneficial interaction, and finally to a one-sided exploitation. This change, however, has not occurred without some debate (Gorlick et al. 1978, Hobson 1969) because researchers still know little about the evolution of these symbioses. Cleaning involves the removal by a cleaning organism of ectoparasites, diseased or injured tissue, or other particles from the external surfaces or even the buccal cavity of another cooperating organism, hereafter called the client. Although this definition of cleaning is generally accepted (Losey 1987), the extent of the apparent cooperation is debatable and in no case have the net fitness benefits obtained by the participants been properly quantified. Such quantification also challenges students of other apparently mutualistic associations (Cushman and Beattie 1991). Understanding the proximate and ultimate causes of cleaning symbioses is of more than mere theoretical importance. For instance, fish that can clean have recently been used successfully for the control of ectoparasites on commercially farmed fish (e.g., Bjordal 1991, Cowell et al. 1993) and are viewed as a promising alternative to the use of chemicals (Pike 1989). However, what determines the efficiency of cleaners and their compatibility with certain client species is not yet fully understood. In this article, we review the current knowledge and ideas on cleaning symbioses, focusing on their adaptive significance. Although the literature emphasizes cleaning among fish, we discuss issues relevant to all taxa involved in cleaning symbioses.

Tactile stimulation lowers stress in fish

In humans, physical stimulation, such as massage therapy, reduces stress and has demonstrable health benefits. Grooming in primates may have similar effects but it remains unclear whether the positive effects are due to physical contact or to its social value. Here we show that physical stimulation reduces stress in a coral reef fish, the surgeonfish Ctenochaetus striatus. These fish regularly visit cleaner wrasses Labroides dimidiatus to have ectoparasites removed. The cleanerfish influences client decisions by physically touching the surgeonfish with its pectoral and pelvic fins, a behaviour known as tactile stimulation. We simulated this behaviour by exposing surgeonfish to mechanically moving cleanerfish models. Surgeonfish had significantly lower levels of cortisol when stimulated by moving models compared with controls with access to stationary models. Our results show that physical contact alone, without a social aspect, is enough to produce fitness-enhancing benefits, a situation so far only demonstrated in humans.

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.