Cleaner Fish Labroides Research Articles

A marine cleaning mutualism provides new insights in biological market dynamics.

Most mutually beneficial social interactions (cooperation within species, mutualism between species) involve some degree of partner choice. In an analogy to economic theory as applied to human trading practices, biological market theory (BMT) focuses on how partner choice affects payoff distributions among non-human traders. BMT has inspired a great diversity of research, including research on the mutualism between cleaner fish Labroides dimidiatus and other marine fish, their 'clients'. In this mutualism, clients have ectoparasites removed and cleaners obtain food in return. We use the available data on L. dimidiatus cleaner-client interactions to identify avenues for future expansion of BMT. We focus on three main topics, namely how partner quality interacts with supply-to-demand ratios to affect service quality, the role of threats and forms of forceful intervention, and the potential role of cognition. We consider it essential to identify the specifics of each biological market as a basis for the development of more sophisticated BMT models. This article is part of the theme issue 'Half a century of evolutionary games: a synthesis of theory, application and future directions'.

Indirect effects of cleaner fish Labroides dimidiatus on fish grazing per reef area and benthic community structure

Grazing fishes farm algae, and consume algae, detritus and sediment and consequently differentially modify benthic communities. Manipulations of cleaner fish Labroides dimidiatus on reefs show that cleaners affect fish abundance differently according to grazer functional group. Accordingly, whether reefs are grazed differently, with consequences for the benthos (fouling material tile−1), was tested using reefs kept free of L. dimidiatus for 10 years compared with undisturbed control reefs. We recorded on video the grazing density (bites tile−1 h−1 reef−1) on settlement tiles and the natural benthos (roving fishes only), according to territorial algal farmer (Pomacentridae) and roving grazer (Acanthuridae, Labridae, Siganidae) functional groups, and measured the accumulation of fouling material tile−1 after 10 months. Grazing density on tiles (dominated by ‘indeterminate’ farmers, and roving ‘sediment-removing’ detritivore Ctenochaetus striatus) and the natural benthos (dominated by Ct. striatus and other grazers) was not measurably affected by cleaner presence. The composition of fouling material (dominated by detritus > turf algae > sediment > other) and organic and inorganic dry weight of material tile−1 were also not measurably affected by cleaner presence. This points to resilience of the benthic community to loss of cleaners. The likely complex interactions between cleaner fish presence, grazer abundance and mobility, and the often-opposite effects of territorial farmers and roving grazers on the benthos underscore the challenge in determining indirect effects of cleaners on benthic community structure. However, a lack of cleaners has negative ramifications for fish populations and physiology and thus their loss remains problematic for client fishes.

Cleaner Fish Labroides dimidiatus Presence Does Not Indirectly Affect Demersal Zooplankton

Coral reef mutualisms involve complex trophic ecological relationships that produce indirect effects. Excluding mutualistic cleaner fish Labroides dimidiatus from reefs indirectly increases the abundance of many fishes and reduces demersal stages of their ectoparasitic prey (gnathiid isopods). Whether cleaners affect populations of planktivorous fishes that consume demersal zooplankton, and consequently indirectly affect the rest of the demersal zooplankton community — via presumed changes in planktivory — is unknown. Therefore, using a long-term cleaner fish manipulation on patch reefs (July 2000 to December 2012, Great Barrier Reef), we tested whether cleaner treatment (removal or control) affects planktivorous fish abundance and diversity, and demersal zooplankton biomass, abundance, and diversity. Fish surveys, 9 and 12 years after removing cleaners revealed fewer fish on removal compared to control reefs for one of the three most abundant planktivores, but not total abundance (Pomacentridae, 26 species), diversity, and composition. Emerging zooplankton were sampled during the day and night over nine sampling trips across 12 years. There was no effect of cleaner treatment on post-removal values, compared with pre-removal values in July 2000, for zooplankton biomass, abundance, diversity, and composition (34 taxa). Zooplankton abundance showed no diel differences, but diversity, and occasionally biomass, were higher at night. Zooplankton composition also showed diel differences, with three taxa contributing the most to this dissimilarity [Cirripeda nauplii, Facetotecta (Arthopoda), Oikopleuridae (Chordata)]. Zooplankton diversity did not differ among times, abundance was higher in January 2002 relative to July 2000, and composition differed among all times. The lack of detectable indirect effects of cleaner fish presence on zooplankton (non-gnathiid) may partly be due to cleaners’ variable effect on planktivorous fish abundance, but also the result of invertebrate planktivory and other processes that affect zooplankton populations not investigated here. Nevertheless, the pronounced diel and temporal changes in zooplankton observed likely influence coral reef trophic interactions.

No evidence for general intelligence in a fish

AbstractThe average mammal or bird has a roughly ten times larger brain relative to body size than the average ectotherm vertebrate. It has been surprisingly challenging to determine how this translates into increased cognitive performance. In particular, it is unclear whether the brain size differences translate into qualitative differences in specific cognitive abilities. Here, we provide a first exploratory study to examine the possibility that the larger brains of endotherms support a different organisation of information processing, rather than specific differences in cognitive processes. In mammals, individual performance across domain‐general cognitive tasks is positively correlated, resulting in the psychometric factor g. The value of g is positively correlated with brain size. We tested wild‐caught female cleaner fish Labroides dimidiatus, known for its highly sophisticated social behaviour, in four ecologically nonrelevant cognitive tasks that have been used to varying degrees to assess g in mammals. Cleaner fish solved three of these four tasks, flexibility (reversal learning), self‐control (detour around an obstacle) and numerical competence (simultaneous two‐choice task), while also providing enough interindividual variation to test for g. They did not perform above chance levels in the fourth task, which tested for object permanence. For the three retained tasks, individual performance did not load positively on one principal component. Furthermore, all pairwise correlation coefficients were close to zero. These negative results contradict a frequent criticism of g studies, which proposes that g is a default result of how brains are designed. Rather, the results provide a first indication that endotherm and ectotherm vertebrates may process cognitive tasks in fundamentally different ways due to differences in brain organisation. Our relatively low number of experiments compared to mammalian studies enhances this hypothesis, as the probability of finding a g factor by chance would have been higher.

Cleaner wrasse Labroides dimidiatus perform above chance in a "matching-to-sample" experiment.

Concept learning have been studied widely in non-human animal species within or not an ecological context. Here we tested whether cleaner fish Labroides dimidiatus, which show generalised rule learning in an ecologically relevant context; they generalise that any predator may provide protection from being chased by other fish; can also learn a general concept when presented with abstract cues. We tested for this ability in the matching-to-sample task. In this task, a sample is shown first, and then the subject needs to choose the matching sample over a simultaneously presented different one in order to obtain a food reward. We used the most general form of the task, using each stimulus only once in a total of 200 trials. As a group, the six subjects performed above chance, and four individuals eventually reached learning criteria. However, individual performance was rather unstable, yielding overall only 57% correct choices. These results add to the growing literature that ectotherms show the ability of abstract concept learning, though the lack of stable high performance may indicate quantitative performance differences to endotherms.

Modelling how cleaner fish approach an ephemeral reward task demonstrates a role for ecologically tuned chunking in the evolution of advanced cognition.

What makes cognition “advanced” is an open and not precisely defined question. One perspective involves increasing the complexity of associative learning, from conditioning to learning sequences of events (“chaining”) to representing various cue combinations as “chunks.” Here we develop a weighted graph model to study the mechanism enabling chunking ability and the conditions for its evolution and success, based on the ecology of the cleaner fish Labroides dimidiatus. In some environments, cleaners must learn to serve visitor clients before resident clients, because a visitor leaves if not attended while a resident waits for service. This challenge has been captured in various versions of the ephemeral reward task, which has been proven difficult for a range of cognitively capable species. We show that chaining is the minimal requirement for solving this task in its common simplified laboratory format that involves repeated simultaneous exposure to an ephemeral and permanent food source. Adding ephemeral–ephemeral and permanent–permanent combinations, as cleaners face in the wild, requires individuals to have chunking abilities to solve the task. Importantly, chunking parameters need to be calibrated to ecological conditions in order to produce adaptive decisions. Thus, it is the fine-tuning of this ability, which may be the major target of selection during the evolution of advanced associative learning.

Relative Brain Size and Cognitive Equivalence in Fishes

Scientists have long struggled to establish how larger brains translate into higher cognitive performance across species. While absolute brain size often yields high predictive power of performance, its positive correlation with body size warrants some level of correction. It is expected that larger brains are needed to control larger bodies without any changes in cognitive performance. Potentially, the mean value of intraspecific brain-body slopes provides the best available estimate for an interspecific correction factor. For example, in primates, including humans, an increase in body size translates into an increase in brain size without changes in cognitive performance. Here, we provide the first evaluation of this hypothesis for another clade, teleost fishes. First, we obtained a mean intraspecific brain-body regression slope of 0.46 (albeit with a relatively large range of 0.26–0.79) from a dataset of 51 species, with at least 10 wild adult specimens per species. This mean intraspecific slope value (0.46) is similar to that of the encephalisation quotient reported for teleosts (0.5), which can be used to predict mean cognitive performance in fishes. Importantly, such a mean value (0.46) is much higher than in endothermic vertebrate species (≤0.3). Second, we used wild-caught adult cleaner fish Labroides dimidiatus as a case study to test whether variation in individual cognitive performance can be explained by body size. We first obtained the brain-body regression slope for this species from two different datasets, which gave slope values of 0.58 (MRI scan data) and 0.47 (dissection data). Then, we used another dataset involving 69 adult cleaners different from those tested for their brain-body slope. We found that cognitive performance from four different tasks that estimated their learning, numerical, and inhibitory control abilities was not significantly associated with body size. These results suggest that the intraspecific brain-body slope captures cognitive equivalence for this species. That is, individuals that are on the brain-body regression line are cognitively equal. While rather preliminary, our results suggest that fish and mammalian brain organisations are fundamentally different, resulting in different intra- and interspecific slopes of cognitive equivalence.

Sex differences in the cognitive abilities of a sex-changing fish species Labroides dimidiatus.

Males and females of the same species are known to differ at least in some cognitive domains, but such differences are not systematic across species. As a consequence, it remains unclear whether reported differences generally reflect adaptive adjustments to diverging selective pressures, or whether differences are mere side products of physiological differences necessary for reproduction. Here, we show that sex differences in cognition occur even in a sex-changing species, a protogynous hermaphroditic species where all males have previously been females. We tested male and female cleaner fish Labroides dimidiatus in four cognitive tasks to evaluate their learning and inhibitory control abilities first in an abstract presentation of the tasks, then in more ecologically relevant contexts. The results showed that males were better learners than females in the two learning tasks (i.e. reversal learning as an abstract task and a food quantity assessment task as an ecologically relevant task). Conversely, females showed enhanced abilities compared with males in the abstract inhibitory control task (i.e. detour task); but both sexes performed equally in the ecologically relevant inhibitory control task (i.e. ‘audience effect’ task). Hence, sex-changing species may offer unique opportunities to study proximate and/or ultimate causes underlying sex differences in cognitive abilities.

Cleaner fish and other wrasse match primates in their ability to delay gratification

Humans are outstanding in their ability to achieve mutual cooperation for direct benefits. One often-quoted factor driving our unique cooperation skills is our ability to delay gratification for future benefits, which is supposedly linked to our advanced cognitive abilities relative to other species. The established experimental paradigm used to test delayed gratification in primates and birds is to give subjects access to a small food reward, which can be exchanged for a larger (quantitative task) or better quality (qualitative task) food reward after a time delay. Here we used this paradigm to test primarily the cleaner fish Labroides dimidiatus for its ability to delay gratification. The specific ecology of cleaners makes them ideal candidates for this task: cleaners remove ectoparasites from visiting ‘client’ reef fish although they prefer to eat client mucus. This eating against preference is equivalent to delayed gratification as clients that have their ectoparasites removed (as opposed to their mucus) will both stay longer with a specific cleaner and return to it for later inspection. Cleaners performed very well in the quantitative task, i.e. similarly to monkeys. In contrast, they performed poorly if the delayed reward was of higher quality. Using the quantitative task to test other wrasse species, we found that another cleaner species and noncleaner wrasse also performed well, the latter despite no evidence that they need such ability to cooperate in nature. However, only the two cleaner species showed evidence for making decisions early on about whether to wait or to directly eat the immediate reward. We conclude that the ability to delay gratification does not warrant advanced cognitive abilities that require endotherm-specific brain morphology, although the underlying mechanisms vary between species. • Ability to delay gratification supposedly indicates advanced cognitive capacities. • Wrasse performed similarly to monkeys in a quantitative delayed reward task. • Cleaner fish showed evidence for anticipation as few primates do. • Ectotherms may have a different perception of time compared to endotherms.

Effects of the cleaner fish Labroides dimidiatus on grazing fishes and coral reef benthos

Territorial and roving grazing fishes farm, and feed on, algae, sediment, or detritus, thus exerting different influences on benthic community structure, and are common clients of cleaner fish. Whether cleaners affect grazing-fish diversity and abundance, and indirectly the benthos, was tested using reefs maintained free of the bluestreak cleaner wrasseLabroides dimidiatusfor 8.5 yr (removals) compared with controls. We quantified fish abundance per grazing functional group, foraging rates of roving grazers, cleaning rates of roving grazers byL. dimidiatus, reef benthos composition, and fouling material on settlement tiles. Abundances of ‘intensive’ and ‘extensive’ territorial farmers, non-farmers, parrotfishes andAcanthurusspp. were lower on removal than control reefs, but this was not the case for ‘indeterminate’ farmers andCtenochaetus striatus. Foraging rates ofAcanthurusspp. andC. striatuswere unaffected by cleaner presence or cleaning duration. This suggests some robustness of the grazers’ foraging behaviour to loss of cleaners.Acanthurusspp. foraged predominantly on sediment and detritus, whereasC. striatusand parrotfishes grazed over algal turfs. Nevertheless, benthic community structure and amount of organic and inorganic material that accumulated over 3.5 mo on tiles were not affected by cleaner presence. Thus, despite greater abundances of many roving grazers, and consequently higher grazing rates being linked to the presence of cleaners, the benthos was not detectably affected by cleaners. This reveals that the positive effect of cleaners on fish abundance is not associated with a subsequent change in the benthos as predicted. Rather, it suggests a resilience of benthic community structure to cleaner-fish loss, possibly related to multiple antagonistic effects of different grazer functional groups. However, losing cleaners remains a problem for reefs, as the lack of cleaning has adverse consequences for fish physiology and populations.

Long‐term memory retention in a wild fish species Labroides dimidiatus eleven months after an aversive event

AbstractMemory is essential to enhance future survival and reproduction as it helps in storing and retrieving useful information to solve particular environmental problems. However, we lack quantitative evidence on how far animals in the wild can maintain given information for extended periods without reinforcement. Here, we document correlative evidence of cleaner fish Labroides dimidiatus remembering being caught in a barrier net for up to 11 months. In 2015, about 60% of cleaners from one large isolated reef had been used for laboratory experiments and then returned to their site of capture. Eleven months later, 50% of cleaners at the same site showed an unusual hiding response to the placement of the barrier net, in contrast to three control sites where no cleaners had been caught during the last 2 years. The results suggest that a single highly aversive event (i.e., being caught in a barrier net) resulted in cleaners storing long‐term crucial information that allowed them to avoid being caught again. Our results further our knowledge of fish cognitive capacities and long‐term memory retention.

Changes in local free-living parasite populations in response to cleaner manipulation over 12years.

Predation on parasites is an important ecological process, but few experimental studies have examined the long-term impacts on the prey. Cleaner fish prey upon large numbers and selectively feed on the larger individuals of the ectoparasitic stage of gnathiid isopods. Removal of cleaner fish Labroides dimidiatus for 1.5-12.5years negatively affects coral reef fishes, but the mechanism is unclear. A reduction in local parasite populations or the size of individual parasites would benefit all susceptible fishes. We tested whether cleaner presence reduces local gnathiid populations using 18 patch-reefs distributed between two sites (both at Lizard Island, Great Barrier Reef) which were maintained cleaner-free or undisturbed for 12years. Using emergence traps (1m2), free-living gnathiid stages were sampled before and after cleaner fish were removed during the day and night, up to 11 times over the course of the experiment. There were effects of the removal in the predicted direction, driven largely by the response at one site over the other involving 200% more gnathiids, but manifested only in the daytime sampling after 4months. There was also a main effect (36%) for the shared sample dates at both sites after 12years. Gnathiid size occasionally differed with cleaner presence, but in no consistent way over time. Contrary to our predictions, changes in free-living gnathiid population numbers and their size structure rarely reflected the changes in fish populations and individuals observed on cleaner-free reefs. Therefore, evidence that this predator alone regulates gnathiids remains limited, suggesting other contributing processes are involved.

Estradiol shapes mutualistic behaviour of female cleaner fish (Labroides dimidiatus - Valenciennes, 1839): Potential implications of environmental disturbance

The presence of endocrine-derived compounds in the environment occurs due to a myriad of human or industrial activity and can disrupt the endocrine system of animals, including fish. One important group of endocrine disruptors are the estrogens, such as 17-β estradiol (E2, estradiol). Estrogens are gonadal steroid hormones, able to be influential even in small concentrations. Here, we demonstrate that E2 is linked to female’ decisions made by an important coral reef species, the cleaner fish Labroides dimidiatus, during interactions with other reef fishes (known as clients). E2 treatment in natural conditions interfered directly in the cooperative relationships, by increasing cleaners’ willingness to interact with clients, providing greater amounts of physical contact to their fish partners. We discuss the meaning of the observed behavioural disruption produced by E2, which by affecting a key species (cleaners) may produce a cascade impact in the aquatic ecosystem.

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.

Cleaner fish Labroides dimidiatus discriminate numbers but fail a mental number line test.

Several species of primates, including humans, possess a spontaneous spatial mental arrangement (i.e. mental number line MNL) of increasing numbers or continuous quantities from left to right. This cognitive process has recently been documented in domestic chicken in a spatial-numerical task, opening the possibility that MNL is a cognitive capacity that has been conserved across vertebrate taxa. In this scenario, fish might possess the MNL as well. Here we investigated whether cleaner fish Labroides dimidiatus show evidence for MNL in two experiments. In Experiment I, we tested fish's abilities in number discrimination, presenting simultaneously either small (2 vs 5) or large (5 vs 8) continuous quantities where one quantity was systematically rewarded. Experiment II used a protocol of an MNL task similar to the study on chickens. We trained cleaners with a target number (i.e. 5 elements), then we presented them with an identical pair of panels depicting either 2 elements or 8 elements, and we recorded their spontaneous choice for the left or right panel on each presentation. Cleaner fish showed high abilities in discriminating small and large numbers in Experiment I. Importantly, cleaners achieved this discrimination using numerical cues instead of non-numerical cues such as the cumulative surface area, density, and overall space. In contrast, cleaners did not allocate continuous quantities to space in Experiment II. Our findings suggest that cleaner fish possess numbering skills but they do not have an MNL. While similar studies on animals from various clades are needed to trace the evolution of MNL within vertebrates, our results suggest that this cognitive process might not be a capacity conserved across all vertebrate taxa.

The arginine-vasotocin and serotonergic systems affect interspecific social behaviour of client fish in marine cleaning mutualism

Many species engage in mutualistic relationships with other species. The physiological mechanisms that affect the course of such social interactions are little understood. In the cleaning mutualism, cleaner fish Labroides dimidiatus do not always act cooperatively by eating ectoparasites, but sometimes cheat by taking bites of mucus from so-called “client” reef fish. The physiological mechanisms in these interspecific interactions, however, are little studied. Here, we focussed on three neuromodulator systems known to play important roles in intraspecific social behaviour of vertebrates to examine their role in clients' interspecific behaviour. We subjected the client fish Scolopsis bilineatus to ectoparasites and the exogenous manipulation of the vasotocin (AVT), isotocin (IT) and serotonin systems to test how this affects client willingness to seek cleaning and client aggression towards cleaners. We found that a single dose of AVT agonist and a selective antagonist caused clients to seek proximity to cleaners, independently of ectoparasite infection. In contrast, in a direct encounter task, the selective blocker of serotonin 5HT2A/2C receptors, Ketanserin (KET), made client reef fish more aggressive towards cleaners in the absence of cleaners' bites of mucus. IT did not yield any significant effects. Our results suggest that the AVT system plays a role in social affiliation towards an interspecific partner, while the serotonin system affects clients' acceptance of level of proximity to cleaner fish during interactions. These two systems, therefore, were apparently co-opted from intraspecific social interactions to affect the course of interspecific ones also.

Cleaning up the biogeography of Labroides dimidiatus using phylogenetics and morphometrics

Cleaner fishes are some of the most conspicuous organisms on coral reefs due to their behaviour and prominent body pattern, consisting of a lateral stripe and blue/yellow colouration. All obligate cleaner fishes share this body stripe pattern, which is an important signal for attracting client fishes. However, variability in the cleaning signal of the cleaner fish Labroides dimidiatus has been documented across its range. Here, we investigate the geographic distribution of cleaner signal polymorphisms in L. dimidiatus and contrast this to phylogeographic variation in mitochondrial (mt) DNA. We used samples from 12 sites for genetic analyses, encompassing much of L. dimidiatus’ range from the Red Sea to Fiji. We obtained morphometric measures of the cleaner signal body stripe width from individuals among six of the sites and qualitatively grouped tail stripe shape. mtDNA control region sequences were used for phylogenetic and population genetic analyses. We found that body stripe width was significantly correlated with tail stripe shape and geographical location, with Indian Ocean populations differing in morphology from western Pacific populations. L. dimidiatus haplotypes formed two reciprocally monophyletic clades, although in contrast to morphology, Japanese cleaner fish fell within the same clade as Indian Ocean cleaner fish and both clade types were sympatric in Papua New Guinea. An additional novel finding of our research was that the inclusion of two closely related cleaner fish species, Labroides pectoralis and Labroides bicolor, in the phylogenetic analysis rendered L. dimidiatus polyphyletic. Overall, the findings suggest the diversity within L. dimidiatus is underestimated.

Ultraviolet-B Wavelengths Regulate Changes in UV Absorption of Cleaner Fish Labroides dimidiatus Mucus

High-energy wavelengths in the ultraviolet-B (UVB, 280-315 nm) and the UVA (315-400-nm) portion of the spectrum are harmful to terrestrial and aquatic organisms. Interestingly, UVA is also involved in the repair of UV induced damage. Organisms living in shallow coral reef environments possess UV absorbing compounds, such as mycosporine-like amino acids, to protect them from UV radiation. While it has been demonstrated that exposure to UV (280-400 nm) affects the UV absorbance of fish mucus, whether the effects of UV exposure vary between UVB and UVA wavelengths is not known. Therefore, we investigated whether the UVB, UVA, or photosynthetically active radiation (PAR, 400-700 nm) portions of the spectrum affected the UV absorbance of epithelial mucus and Fulton’s body condition index of the cleaner fish Labroides dimidiatus. We also compared field-measured UV absorbance with laboratory based high-performance liquid chromatography measurements of mycosporine-like amino acid concentrations. After 1 week, we found that the UV absorbance of epithelial mucus was higher in the UVB+UVA+PAR treatment compared with the UVA+PAR and PAR only treatments; after 2 and 3 weeks, however, differences between treatments were not detected. After 3 weeks, Fulton’s body condition index was lower for fish in the UVB+UVA+PAR compared with PAR and UVA+PAR treatments; furthermore, all experimentally treated fish had a lower Fulton’s body condition index than did freshly caught fish. Finally, we found a decrease with depth in the UV absorbance of mucus of wild-caught fish. This study suggests that the increase in UV absorbance of fish mucus in response to increased overall UV levels is a function of the UVB portion of the spectrum. This has important implications for the ability of cleaner fish and other fishes to adjust their mucus UV protection in response to variations in environmental UV exposure.

Potential effects of fishing on cleaning interactions in a tropical reef

We investigated the effect of fishing on the behavior and abundance of the cleaner fish Labroides dimidiatus on the Great Barrier Reef, Australia, by comparing cleaner fish density (underwater visual census) and behavior (focal animal observations) at a fished and a no-take site. Cleaner fish density, as well as the number of individuals and species cleaned, did not differ significantly between sites; however, L. dimidiatus spent more time interacting (physical contact involving feeding bites) with individual clients at the no-take site, indicating that fishing can indirectly affect mutualistic interactions on tropical reefs.

Enhanced colonization success and competition associated with conspecifics in cleaner fish Labroides dimidiatus juveniles

The cleaner fish Labroides dimidiatus affects the abundance of many fishes, including their juveniles, yet how they affect the post-settlement processes of conspecifics remains poorly known. Using a long-term experiment, where L. dimidiatus were regularly removed from seven patch reefs (removals) for 10 years or left undisturbed (controls) on nine, the effect of conspecifics’ presence on recently settled L. dimidiatus juveniles and the relationship between juvenile and adult abundance on control reefs were examined. Repeated sampling 4–40 months after manipulating L. dimidiatus revealed that the abundance of juveniles on removals, compared with controls reefs, was 72 % (95 % CI = 65–79 %) lower; this effect did not vary over time. Thus, decreased colonization was associated with resident conspecific absence and this effect was present after 4 months. Since other studies found 4 months of cleaner absence was too short to affect client abundance—a factor also known to enhance L. dimidiatus colonization—it was likely not involved here. Over 10 years, individual control reefs were almost always occupied by at least one adult (89–100 % of times sampled); but in summer, when L. dimidiatus colonization was highest, juvenile abundance was negatively related with adult abundance at one of two sites, with the expected number of juveniles decreasing by 67 % (95 % CI = 51–83 %) with each additional adult. This suggests a deleterious effect of adults on juveniles at one site, such as competition. Enhanced colonization of juveniles associated with adult presence may partly explain the relative permanence of fish cleaning stations.