The rate at which parasites (mainly gnathiid isopod larvae) were removed from fish by the cleaner wrasse Labroides dimidiatus was investigated. To examine the effect of this parasite removal on the parasites of fish, the number of parasites removed per individual host fish Hemigyrnnus melapterus per day was estimated and compared to the infection, rate and abundance of gnathiids on H. melapterus. The study was conducted at Lizard Island, Great Barrier Reef, Australia, using a comblnation of observations of the feeding rates of cleaners, estimates of how much time lndividual hosts spend being cleaned, cleaner fish stomach content analyses, and a gnathiid manipulation experiment. The frequency and duration of inspection by L. dimidiatus were measured to provide an estimate of the feeding rate. lndividual L. dimidiatus spent on average 256 + 11 (SE) min d-' inspecting 2297 + 83 fish.L. dlmldiatcis consumed a large number of parasites (1218 k 118, mainly gnathiid isopods) each day.The estimated predation rate by L. dirnidiatus was 4 . 8 t 0.4 parasites per minute of inspection or 0.5 + 0.05 parasites per inspection. The infection rate of gnathiids onto fish was high, with reduced gnathiid loads (by about 50%) on fish returning to levels similar to control fish within 1 to 6 d. These high infection rates suggest that a significant proportion of gnathiids removed by cleaner fish are quickly replaced. The high predation rate relative to the number of gnathiids on fish and their infection rate shows that cleaner fish have an effect on the abundance of gnathiids on fish.
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.
Cleaning symbiosis has been documented extensively in the marine environment over the past 50 years. We estimate global cleaner diversity comprises 208 fish species from 106 genera representing 36 families and 51 shrimp species from 11 genera representing six families. Cleaning symbiosis as originally defined is amended to highlight communication between client and cleaner as the catalyst for cooperation and to separate cleaning symbiosis from incidental cleaning, which is a separate mutualism preceded by no communication. Moreover, we propose the term ‘dedicated’ to replace ‘obligate’ to describe a committed cleaning lifestyle. Marine cleaner fishes have dominated the cleaning symbiosis literature, with comparatively little focus given to shrimp. The engagement of shrimp in cleaning activities has been considered contentious because there is little empirical evidence. Plasticity exists in the use of ‘cleaner shrimp’ in the current literature, with the potential to cause significant confusion. Indeed, this term has been used incorrectly for the shrimp Infraorder Stenopodidea, involving three families, Stenopodidae, Palaemonidae and Hippolytidae, and to represent all members of Lysmata and Stenopus. Caution is expressed in the use of grey literature and anecdotal observations to generate data on cleaning interactions, due to the presence of species complexes. Interest in cleaning organisms as biological controls in aquaculture is increasing due to their value as an alternative to various chemical ectoparasite controls. Reports of the importance of cleaner organisms in maintaining a healthy reef ecosystem has also been increasing and we review the current biological knowledge on cleaner organisms, highlighting areas that are understudied.
Individuals from 11 fish species were followed and the number of times and duration that fish were inspected by the cleaner wrasse Labroides dimidiatus were recorded around Lizard Island, Great Barrier Reef. The frequency and duration of inspection were positively correlated with the mean parasite load and mean surface area of the 11 fish species. Surface area, however, explained slightly more of the variation in inspection frequency and duration among species than did ectoparasite load. This suggests surface area may be useful for predicting the cleaning rates of fish species. When the frequency and duration of inspection were corrected for mean surface area and mean ectoparasite load, differences among fish species disappeared. Observations of 3 size classes from l fish species, Hemigymnus melapterus, revealed that larger fish, w h~c h have more parasites, were inspected more often and for longer periods than smaller fish with fewer parasites. The fact that fish with more parasites are cleaned more suggests that parasites play an important role in fish cleaning interactions.
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.
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