Does client size affect cleaner fish choice of client? An empirical test using client fish models

To determine whether the choice of client fishes in the cleaner fish Labroides dimidiatus was influenced by client size, cleaner fish were given a choice of equal amount of food spread on large and small client redfin butterflyfish Chaetodon trifasciatus models. All large models received bites from cleaners compared to 27% for small models. Seventy‐nine per cent of cleaners took their first bite from the large fish model. The results suggest that client size may affect cleaner fish choice.     

Oceanic sharks clean at coastal seamount

Interactions between pelagic thresher sharks (Alopias pelagicus) and cleaner wrasse were investigated at a seamount in the Philippines. Cleaning associations between sharks and teleosts are poorly understood, but the observable interactions seen at this site may explain why these mainly oceanic sharks regularly venture into shallow coastal waters where they are vulnerable to disturbance from human activity. From 1,230 hours of observations recorded by remote video camera between July 2005 and December 2009, 97 cleaner-thresher shark events were analyzed, 19 of which were interrupted. Observations of pelagic thresher sharks interacting with cleaners at the seamount were recorded at all times of day but their frequency declined gradually from morning until evening. Cleaners showed preferences for foraging on specific areas of a thresher shark's body. For all events combined, cleaners were observed to conduct 2,757 inspections, of which 33.9% took place on the shark's pelvis, 23.3% on the pectoral fins, 22.3% on the caudal fin, 8.6% on the body, 8.3% on the head, 2.1% on the dorsal fin, and 1.5% on the gills respectively. Cleaners did not preferentially inspect thresher sharks by time of day or by shark sex, but there was a direct correlation between the amount of time a thresher shark spent at a cleaning station and the number of inspections it received. Thresher shark clients modified their behavior by "circular-stance-swimming," presumably to facilitate cleaner inspections. The cleaner-thresher shark association reflected some of the known behavioral trends in the cleaner-reef teleost system since cleaners appeared to forage selectively on shark clients. Evidence is mounting that in addition to acting as social refuges and foraging grounds for large visiting marine predators, seamounts may also support pelagic ecology by functioning as cleaning stations for oceanic sharks and rays.     

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.     

Cleaner fish use tactile dancing behavior as a preconflict management strategy

The most commonly asked question about cooperative interactions is how they are maintained when cheating is theoretically more profitable. In cleaning interactions, where cleaners remove parasites from apparently cooperating clients, the classical question asked is why cleaner fish can clean piscivorous client fish without being eaten, a problem Trivers used to explain reciprocal altruism. Trivers suggested that predators refrain from eating cleaners only when the repeated removal of parasites by a particular cleaner results in a greater benefit than eating the cleaner. Although several theoretical models have examined cheating behavior in clients, no empirical tests have been done (but see Darcy ). It has been observed that cleaners are susceptible to predation. Thus, cleaners should have evolved strategies to avoid conflict or being eaten. In primates, conflicts are often resolved with conflict or preconflict management behavior. Here, I show 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 preconflict management strategy that enables cleaner fish to avoid conflict with potentially "dangerous" clients.     

Effects of juvenile coral-feeding butterflyfishes on host corals

Corals provide critical settlement habitat for a wide range of coral reef fishes, particularly corallivorous butterflyfishes, which not only settle directly into live corals but also use this coral as an exclusive food source. This study examines the consequences of chronic predation by juvenile coral-feeding butterflyfishes on their specific host corals. Juvenile butterflyfishes had high levels of site fidelity for host corals with 88% (38/43) of small (<30 mm) juveniles of Chaetodon plebeius feeding exclusively from a single host colony. This highly concentrated predation had negative effects on the condition of these colonies, with tissue biomass declining with increasing predation intensity. Declines were consistent across both field observations and a controlled experiment. Coral tissue biomass declined by 26.7, 44.5 and 53.4% in low, medium and high predation intensity treatments. Similarly, a 41.7% difference in coral tissue biomass was observed between colonies that were naturally inhabited by juvenile butterflyfish compared to uninhabited control colonies. Total lipid content of host corals declined by 29–38% across all treatments including controls and was not related to predation intensity; rather, this decline coincided with the mass spawning of corals and the loss of lipid-rich eggs. Although the speed at which lost coral tissue is regenerated and the long-term consequences for growth and reproduction remain unknown, our findings indicate that predation by juvenile butterflyfishes represents a chronic stress to these coral colonies and will have negative energetic consequences for the corals used as settlement habitat.     

Choosy reef fish select cleaner fish that provide high-quality service

Reef fish that actively visit cleaner fish to have parasites and dead or infected tissue removed face two potential problems: they might have to wait while cleaners inspect other clients, and cleaners might feed on healthy body tissue, a behaviour that is referred to as cheating. Individuals of some ‘client’ species have large home ranges, which cover several cleaning stations, while others have small territories or home ranges with access to only one cleaning station. The former can thus choose between cleaners, while the latter cannot. We investigated whether clients with large home ranges change cleaning partners to outplay cleaners against each other to achieve (1) priority of access over clients with no choice at cleaning stations and (2) control over cheating by cleaners. We followed individuals of longnosed parrotfish, Hipposcarus harid, for up to 120 min in their natural environment and noted their interactions with cleaner wrasses, Labroides dimidiatus. Individuals were likely to return to the same cleaning station if the previous interaction had ended without conflict but changed cleaners for the next inspection if they had been either cheated or ignored, at least if the time between two consecutive visits was short. The overall attractiveness of a cleaning station seemed to be largely independent of service quality, which appeared to be similar at all stations. This is the first empirical evidence that the option to change partners is used as a control mechanism to stabilize cooperative behaviour.     

Cleaner fish Labroides dimidiatus manipulate client reef fish by providing tactile stimulation.

The cleaner wrasse Labroides dimidiatus often touches 'client' reef fish dorsal fin areas with its pelvic and pectoral fins. The relative spatial positions of cleaner and client remain constant and the cleaner's head points away from the client's body. Therefore, this behaviour is not compatible with foraging and the removal of client ectoparasites. As clients seek such 'tactile stimulation', it can be classified as an interspecific socio-positive behaviour. Our field observations on 12 cleaners (observation time of 112h) suggest that cleaners use tactile stimulation in order to successfully (i) alter client decisions over how long to stay for an inspection, and (ii) stop clients from fleeing or aggressive chasing of the cleaner in response to a cleaner fish bite that made them jolt. Finally, predatory clients receive tactile stimulation more often than non-predatory clients, which might be interpreted as an extra service that cleaners give to specific partners as pre-conflict management, as these partners would be particularly dangerous if they started a conflict. We therefore propose that cleaner fish use interspecific social strategies, which have so far been reported only from mammals, particularly primates.     

A comparative study of cleaning activity of two reef fishes at Fernando de Noronha Archipelago,tropical West Atlantic

Cleaner fishes are usually classified as obligate or facultative cleaners according to their diet and the extent to which their nutritional requirements in the different ontogenetic stages are gained from cleaning. While obligate cleaners clean throughout their lives and ingest mainly food taken from the clients’ body surface, facultative cleaners clean only as juveniles and have a broader diet. In addition, some facultative cleaners may experience a relatively higher predation risk, and thus rarely interact with piscivorous fishes. Despite these acknowledged differences, there are very few studies that compare cleaning activity of obligate and facultative cleaners within the same area. Cleaning activity of the obligate cleaner goby Elacatinus cf. randalli and the facultative cleaner wrasse Thalassoma noronhanum were comparatively examined at Fernando de Noronha Archipelago, tropical West Atlantic. The client assemblage attended by the two cleaners differed, as the goby attended a slightly greater diversity of species (22), mostly piscivores and zoobenthivores, and the wrasse attended fewer species (19), mostly planktivores. Chromis multilineata was the most common client species of both cleaners, although body size (which is expected to be positively correlated to clients’ ectoparasite load) of C. multilineata individuals attended by the goby was larger than that of the individuals attended by the wrasse. Despite such differences, T. noronhanum showed a surprisingly species-rich client assemblage when compared with other cleaners of the genus Thalassoma. In addition, the frequency and time spent on cleaning interactions, as well as the number of client species attended per 10-min period, was similar for both cleaner species, which indicate that they have important yet complimentary ecological roles in the reef community at Fernando de Noronha Archipelago.     

A decrease in the abundance and strategic sophistication of cleaner fish after environmental perturbations

Coral reef ecosystems are declining worldwide and under foreseeable threat due to climate change, resulting in significant changes in reef communities. It is unknown, however, how such community changes impact interspecific interactions. Recent extreme weather events affecting the Great Barrier Reef, that is, consecutive cyclones and the 2016 El Niño event, allowed us to explore potential consequences in the mutualistic interactions involving cleaner fish Labroides dimidiatus (hereafter “cleaner”). After the perturbations, cleaner densities were reduced by 80%, disproportionally compared to the variety of reef fish clients from which cleaners remove ectoparasites. Consequently, shifts in supply and demand yielded an increase in the clients’ demand for cleaning. Therefore, clients became less selective toward cleaners, whereas cleaners were able to choose from a multitude of partners. In parallel, we found a significant decline in the ability of cleaners to manage their reputation and to learn to prioritize ephemeral food sources to maximize food intake in laboratory experiments. In other words, cleaners failed to display the previously documented strategic sophistication that made this species a prime example for fish intelligence. In conclusion, low population densities may cause various effects on individual behavior, and as a consequence, interspecific interactions. At the same time, our data suggest that a recovery of population densities would cause a recovery of previously described interaction patterns and cleaner strategic sophistication within the lifetime of individuals.     

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.     

Multiple cleaner species provide simultaneous services to coral reef fish clients

Cleaning symbioses on tropical coral reefs are typically documented between two species: a single client fish and one or more conspecific cleaners. However, multiple cleaner species living sympatrically in the Caribbean have been anecdotally reported to simultaneously clean the same client. Nothing is known about the patterns and processes driving these interactions, which may differ from those involving a single cleaner species. Here, we used remote underwater videography on three reefs in Honduras to record simultaneous cleaning interactions involving Pederson''s cleaner shrimp (Ancylomenes pedersoni) and cleaner gobies (Elacatinus spp.). A pilot study on adjacent shrimp and goby stations found interactions were always initiated by shrimp. A larger, multi-year dataset shows cleaner gobies joined 28% of all interactions initiated at A. pedersoni cleaning stations with cleaner gobies residing nearby. Client body size significantly predicted simultaneous cleaning interactions, with 45% of interactions simultaneous for clients greater than 20 cm total body length compared with only 8% for clients less than 20 cm. We also found that simultaneous cleaning interactions lasted over twice as long as shrimp-only interactions. We propose these novel multi-species interactions to be an ideal model system to explore broader questions about coexistence, niche overlap and functional redundancy among sympatric cleaner species.     

Predation risk in tadpole populations shapes behavioural responses of prey but not strength of trait‐mediated indirect interactions

Prey animals often respond to predators by reducing activity levels. This can produce a trait‐mediated indirect interaction (TMII) between predators and prey resources, whereby reduced foraging by prey in the presence of a predator causes an increase in prey resources. TMIIs play important roles in structuring communities, and it is important to understand factors that determine their strength. One such influence may be behavioural variation in the prey species, with indirect effects of predators being stronger within populations that are more responsive to the presence of a predator. We tested 1) whether the behavioural responsiveness of populations of wood frog tadpoles to predator cues was related to the predation risk in their native ponds, and 2) whether more responsive tadpoles yielded stronger TMIIs. To do this, we 1) measured the activity of tadpoles from 18 populations in mesocosms with and without caged predators, and 2) measured changes in the biomass of periphyton (the tadpoles’ diet) between predator treatments for each population. We found that tadpoles from higher predation risk ponds reduced their time outside refuges more in the presence of predators and tended to move less when visible, suggesting possible local adaptation to predation regimes. Though the presence of predators generally resulted in higher periphyton biomass – a TMII – there was no evidence that the strength of this TMII was affected by variation in tadpole behaviour. Foraging activity and general activity may be decoupled to some extent, enabling high predation risk‐adapted tadpoles to limit the fitness costs of reduced foraging when predators are present.     

Cleaning by the wrasse Thalassoma noronhanum, with two records of predation by its grouper client Cephalopholis fulva

The Noronha wrasse Thalassoma noronhanum was recorded cleaning 19 client fish species at Fernando de Noronha Archipelago, o. north–eastern Brazil. The preferred clients were non–dangerous, mostly planktivorous species, whereas the potentially dangerous, predatory species were rarely cleaned. T. noronhanum acts as a cleaner in two distinct ecological situations, at and outside the cleaning stations, and attends different client species in each of them. Potentially dangerous clients were mostly attended outside the cleaning stations. Many attacks and two instances of predation on the cleaner wrasse by the grouper client Cephalopholis fulva were recorded. The attacks occurred on individual wrasses foraging near the bottom outside the cleaning stations.     

Roving and Service Quality in the Cleaner Wrasse Labroides bicolor

The cleaner wrasse Labroides dimidiatus occupies fixed ‘cleaning stations’ on coral reefs, which ‘client’ reef fish visit repeatedly to have parasites removed. Conflict arises because cleaners prefer to cheat by feeding on client mucus instead of parasites. Clients can prevent L. dimidiatus from always cheating using control mechanisms such as chasing and partner switching, which depend on repeated interactions. These control mechanisms would be undermined in the absence of frequent repeated interactions, if cleaners roved over large areas. Roving behaviour has been anecdotally described for the closely related cleaner wrasse Labroides bicolor. Here we report field data comparing these two species in Moorea, French Polynesia. Our results confirmed that L. bicolor home ranges are much larger than L. dimidiatus home ranges, and showed that cleaning interactions occurred all over the L. bicolor home range: home range of cleaning interactions increased with total home range size. Moreover, we found that cleaner initiation of interactions increased with home range size in L. bicolor, which would give L. bicolor with large home ranges additional leverage to increase cheating. In line with these results, we found that client jolt rate (used as a measure of cheating) was higher among clients of cleaners with large home ranges. Our results emphasise the importance of game structure and control over initiating interactions as parameters in determining the nature of interactions in mutualisms.     

Caribbean Cleaning Gobies Prefer Client Ectoparasites Over Mucus

If cooperation often involves investment, then what specific conditions prevent selection from acting on cheaters that do not invest? The mutualism between the Indo‐Pacific cleaner wrasse Labroides dimidiatus and its reef fish clients has been a model system to study conflicts of interest and their resolution. These cleaners prefer client mucus over ectoparasites – that is, they prefer to cheat – but punishment and partner switching by clients enforce cooperative behaviour by cleaners. By contrast, clients of Caribbean cleaning gobies (Elacatinus spp.) do not to use punishment or partner switching. Here, we test the hypothesis that the behavioural differences between these two cleaner fish systems are caused by differences in cleaner foraging preferences. In foraging choice experiments, we offered broadstripe cleaning gobies Elacatinus prochilos client‐derived parasitic isopods, client mucus and a control food item. The cleaning gobies significantly preferred ectoparasites over mucus or the control item, which contrasts with cleaner wrasses. We propose that the low level of cleaner–client conflict arising from cleaning goby foraging preferences explains the observed lack of strategic partner control behaviour in the clients of cleaning gobies.     

Foraging plasticity in obligate corallivorous Melon butterflyfish across three recently bleached reefs

Because obligate corallivorous butterflyfish feed exclusively on coral polyps, they are particularly sensitive to changes in coral cover and its spatial distribution. To understand how such differences in coral cover influence obligate corallivores, we examined the densities and foraging behavior of Melon butterflyfish Chaetodon trifasciatus across three reefs in the Lakshadweep archipelago. These reefs suffered differential bleaching mortality after the 2010 El Niño Southern Oscillation, resulting in wide variation in coral cover and community composition. Despite these differences, C. trifasciatus were able to persist at similar densities across reefs. However, our analysis of high‐resolution video recordings of multiple focal fish revealed that time budgets, bite rates, and diet selectivity differed significantly. Fish in resource‐poor reefs spent more time moving between coral patches and less time foraging than ones in relatively resource‐rich reefs. We also found that fish in resource‐poor reefs had higher bite rates and were less selective in their foraging. Our results provide novel insights into how obligate corallivores cope with even large differences in resource availability. At a time when we are rapidly losing corals to repeated climate‐induced bleaching events, this flexibility may represent a critical mechanism that enables persistence of obligate corallivores in resource‐poor reefs, even if it does not guarantee longer‐term survival.     

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.     

Susceptibility to predation affects trait-mediated indirect interactions by reversing interspecific competition

Numerous studies indicate that the behavioral responses of prey to the presence of predators can have an important role in structuring assemblages through trait-mediated indirect interactions. Few studies, however, have addressed how relative susceptibility to predation influences such interactions. Here we examine the effect of chemical cues from the common shore crab Carcinus maenas on the foraging behavior of two common intertidal gastropod molluscs. Of the two model consumers studied, Littorina littorea is morphologically more vulnerable to crab predation than Gibbula umbilicalis, and it exhibited greater competitive ability in the absence of predation threat. However, Littorina demonstrated a greater anti-predator response when experimentally exposed to predation cues, resulting in a lower level of foraging. This reversed the competitive interaction, allowing Gibbula substantially increased access to shared resources. Our results demonstrate that the susceptibility of consumers to predation can influence species interactions, and suggest that inter-specific differences in trait-mediated indirect interactions are another mechanism through which non-consumptive predator effects may influence trophic interactions.     

Geographic Variation in the Behaviour of the Cleaner Fish Labroides dimidiatus (Labridae)

Geographical variation in the outcome of interspecific interactions has a range of proximate ecological causes. For instance, cleaning interactions between coral reef fishes can result in benefits for both the cleaner and its clients. However, because both parties can cheat and because the rewards of cheating may depend on the local abundance of ectoparasites on clients, the interaction might range from exploitative to mutualistic. In a comparative analysis of behavioural measures of the association between the cleaner fish Labroides dimidiatus and all its client species, we compared cleaning interactions between two sites on the Great Barrier Reef that differ with respect to mean ectoparasite abundance. At Heron Island, where client fish consistently harbour fewer ectoparasites, client species that tended to pose for cleaners were more likely to receive feeding bites by cleaners than client species that did not pose for cleaners. This was not the case at Lizard Island, where ectoparasites are significantly more abundant. Client fish generally spent more time posing for cleaners at Lizard Island than their conspecifics at Heron Island. However, fish at Heron Island were inspected longer on average by cleaners than conspecifics at Lizard Island, and they incurred more bites and swipes at their sides per unit time from cleaners. These and other differences between the two sites suggest that the local availability of ectoparasites as a food source for cleaners may determine whether clients will seek cleaning, and whether cleaners will feed on parasites or attempt to feed on client mucus. The results suggest that cleaning symbiosis is a mosaic of different outcomes driven by geographical differences in the benefits for both participants.     

Temporal Variation in Cleanerfish and Client Behaviour: Does It Reflect Ectoparasite Availability?

We tested the importance of ectoparasites as the proximate cause of cleaning interactions by comparing the activity of Caribbean cleaning gobies (Elacatinus evelynae) and of their clients during three daily periods (early morning, midday, and late afternoon) in which ectoparasite availability varied naturally. Emergence from the benthos of gnathiid isopod larvae, the main target of cleaning goby predation, was higher at night, when cleaners were inactive, than during the day. As a result, overall ectoparasite loads on client fish tended to be higher in the morning. Inspection bouts by cleaning gobies were longest in the morning, but also at midday when ectoparasite availability on clients was lower. Client fish were observed at cleaning stations most often in the afternoon, when they harboured few ectoparasites, but they were more likely to adopt incitation poses, which increase the likelihood of being cleaned, in the morning than later in the day. Most cleaner and client behaviours therefore did not change predictably in response to natural diurnal variation in ectoparasite availability. Our study suggests that the ultimate and proximate causes of cleaning behaviour need not necessarily coincide.