Cleaning Activity of Juvenile Angelfish, Pomacanthus paru, on the Reefs of the Abrolhos Archipelago, Western South Atlantic

Studies on fish cleaning symbiosis in the tropical western Atlantic concentrate on specialized cleaner gobies and wrasses. On the reefs of the Abrolhos Archipelago, off the eastern Brazilian coast, juvenile french angelfish, Pomacanthus paru, clean a rich and varied community of fish clients. We recorded 31 reef fish species, including large predators such as groupers, jacks, and morays, being serviced by the french angelfish on cleaning stations situated mostly on seagrass flats. The angelfish performs a characteristic fluttering swimming at the station and, during cleaning events, touches the body of the clients with its pelvic fins. Frequency of encounters between the cleaner and its clients do not reflect the local abundance of client species; most of these move from the reefs to the sand flats to be cleaned. We found no correlation between client size and duration of cleaning events. The conspicuous black and yellow pattern, the fluttering swimming, the tenure of cleaning stations, the physical contact with the client, and the varied community of clients, qualify the juveniles of P. paru as specialized cleaners comparable to the gobies of the genus Elacatinus.     

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.     

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.     

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.     

The cost of cleanerfish mimics to their models

In aggressive mimicry, a 'predatory' species resembles a model that is harmless or beneficial to a third species, the 'dupe'. Perhaps the most extraordinary case of aggressive mimicry occurs in Indo‐Pacific cleaning symbioses, where cleaner wrasses (the models) remove ectoparasites from larger fish clients. Several species of fangblennies mimic cleaners in behaviour and coloration. Instead of removing ectoparasites, however, fangblennies tear off fins, skin and scales from unsuspecting clients (the dupes). There is some debate over the extent to which cleanerfish mimics are really mimics because in some populations, the contribution of fish tissue to fangblenny diet is limited. In this study, I examine the impact of the resemblance between bluestriped fangblennies ( Plagiotremus rhinorhynchus ) and its putative model, the juvenile bluestreak cleaner wrasse ( Labroides dimidiatus ), on the model's cleaning activity to test the theoretical prediction that mimics should decrease the fitness of their models. I show that the presence of a bluestripe fangblenny in the vicinity of cleaner wrasses results in significantly lower client visit rates and inspection times compared to cleaners without a fangblenny nearby, and discuss why cleaner wrasses tolerate mimics near 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.     

Whale sharks Rhincodon typus get cleaned by the blue-streak cleaner wrasse Labroides dimidiatus and the moon wrasse Thalassoma lunare in the Philippines

Cleaning interactions are essential for healthy marine ecosystem communities. This study reports the first documentation of the whale shark Rhincodon typus cleaning behaviour in the Indo-West Pacific by two wrasse species, the blue-streak cleaner wrasse Labroides dimidiatus and the moon wrasse Thalassoma lunare in Cebu, Philippines. This study documented 36 cleaning interactions with 14 individual whale sharks. The cleaning interactions appear opportunistic rather than targeted by the sharks, unlike that observed in other species of elasmobranchs. Further work should focus on understanding the drivers of these unique cleaning interactions.     

Daily Cleaning Activity and Diversity of Clients of the Barber Goby, Elacatinus figaro, on Rocky Reefs in Southeastern Brazil

Gobies of the genus Elacatinus are regarded as the most specialised cleaner fishes in the western tropical Atlantic, yet there are no studies on these cleaners in the southern portion of West Atlantic. We studied the diversity of clients and the daily cleaning activity of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil (23–24°S). A total of 34 fish client species in 16 families were recorded over 484 cleaning events. The most frequent clients were damselfishes, Pomacentridae (37.9% of cleaning events) and grunts, Haemulidae (16.9%). Planktivores were the most frequently attended trophic category, and two species in that category accounted for about a half (44%) of the total cleaning events. Size of clients ranged 4.5–55cm and most individuals were medium-sized (12–30cm); as the barber goby ranged 2–4.5cm, clients were 1.5 to 15 times larger than the cleaner was. Cleaning activity started at dawn and ended shortly before nightfall, the highest frequency of interactions occurring at early morning (nocturnal clients) and mid-afternoon (diurnal clients). By midday the frequency of cleaning events decreased and their duration increased. A total of 109±3 cleaning events and 30±1min of cleaning activity were estimated per cleaning station per day, both figures low when compared to those recorded for cleaner fishes in tropical areas of the western Atlantic and Indo-Pacific.     

Cleaning interactions at the only atoll in the South Atlantic

In marine ecosystems, cleaning is a mutualistic relationship in which so-called cleaners remove ectoparasites, diseased tissue, or mucus from the body of their clients, and thus help to maintain a healthy reef community. In spite of its importance in many marine habitats, this interaction remains poorly understood, particularly at oceanic islands. Here, we present the first comprehensive study of cleaning interactions in a reef fish assemblage at Rocas, the only atoll in the South Atlantic. We recorded 318 cleaning events, in which six fish species, including two endemic ones, and two shrimp species acted as cleaners. The clients serviced by these cleaners were 21 bony fish species, one shark and one sea turtle. The cleaner wrasse Thalassoma noronhanum and the cleaner goby Elacatinus phthirophagus were the cleaners with the greatest number of events and species richness of clients. Additionally, 82% of clients in the cleaning events were non-piscivores, and the abundance of both cleaners and clients positively influenced the number of cleaning events (R² = 0.4; p < 0.001). Our results indicate that Rocas atoll has a high species richness of cleaner species despite its small size and highlight the importance of studies of cleaning symbiosis, even in isolated places with low species richness, for a better comprehension of this association in reefs.     

Mutualism promotes site selection in a large marine planktivore

1. Mutualism is a form of symbiosis whereby both parties benefit from the relationship. An example is cleaning symbiosis, which has been observed in terrestrial and marine environments. The most recognized form of marine cleaning symbiosis is that of cleaner fishes and their clients.
2. Cleaner species set up cleaning stations on the reef, and other species seek out their services. However, it is not well understood how the presence of cleaning stations influence movements of large highly mobile species. We examined the role of cleaning stations as a driver of movement and habitat use in a mobile client species.
3. Here, we used a combination of passive acoustic telemetry and in‐water surveys to investigate cleaning station attendance by the reef manta ray Mobula alfredi. We employed a novel approach in the form of a fine‐scale acoustic receiver array set up around a known cleaning area and tagged 42 rays. Within the array, we mapped structural features, surveyed the distribution of cleaner wrasse, and observed the habitat use of the rays.
4. We found manta ray space use was significantly associated with blue‐streak cleaner wrasse Labroides dimidiatus distribution and hard coral substrate. Cleaning interactions dominated their habitat use at this site, taking precedence over other life history traits such as feeding and courtship.
5. This study has demonstrated that cleaning symbiosis is a driver for highly mobile, and otherwise pelagic, species to visit inshore reef environments. We suggest that targeted and long‐term use of specific cleaning stations reflects manta rays having a long‐term memory and cognitive map of some shallow reef environments where quality cleaning is provided. We hypothesize that animals prefer cleaning sites in proximity to productive foraging regions.

     

Size and stripes: how fish clients recognize cleaners

Little is known of how individuals find each other in interspecific mutualisms involving free-living partners. We tested the importance of two factors, namely body size and the presence of a lateral body stripe, in the recognition of cleanerfish by their fish clients. Clients on an Indonesian reef flat readily approached wooden models of the bluestreak cleaner wrasse, Labroides dimidiatus, which varied in size and stripe characteristics. The composition of the clientele of models was not significantly different from that of natural cleaning stations, suggesting that fish visiting the models were seeking to be cleaned. Normal-sized models of cleaner wrasses attracted significantly more clients, which showed more intense interest and stayed with the models for significantly longer, than super-sized models. For normal-sized models, the number of clients increased as the length of the cleaner's lateral stripe increased (from 0, to 44, 67 and 100% of body length). However, there was no effect of stripe length on client numbers for super-sized models. Client interest also did not vary with stripe length for models of either size. Small body size and the presence of a lateral stripe therefore appear to be long-distance signals that their bearer may be a cleaner, but after initial attraction, client interest is maintained by other cues. Alternative short-distance signals may include colour, other visual signals such as cleanerfish dances, or physical contact between cleaner and client.     

Cleaning activity of two Caribbean cleaning gobies: intra- and interspecific comparisons

Sharknose cleaning gobies Elacatinus evelynae were found predominantly in male—female pairs at cleaning stations located almost exclusively on coral heads. By contrast, broadstripe cleaning gobies Elacatinus prochilos were found at cleaning stations on two distinct substrata: coral and sponge, which were linked to marked differences in social behaviour, cleaning activity and diet. Elacatinus prochilos at coral cleaning stations were more frequently solitary or found in small groups, while groups of up to 40 individuals were observed on sponge cleaning stations. Coral-dwelling E. prochilos spent, on average, 25 times longer cleaning and took 16 times more bites on clients than those on sponge, which was reflected in the larger proportion of client-gleaned material in their gut (40% v . <1%). These substratum-linked differences may result from differences in availability of food items at different cleaning stations. Few differences in cleaning activity were found between E. evelynae and coral-dwelling E. prochilos , although the latter contained a higher proportion of client-gleaned items (40% v . 25%). Most coral-dwelling cleaning gobies had ingested fish scales, although the variation among individuals was high (0–81 fish⁻¹). Intra- and interspecific variability in cleaning activity of cleaner fishes implies that cleaning services for clients may vary significantly between cleaning stations.     

Cleaning interactions by gobies on a tropical eastern Pacific coral reef

The present study describes the cleaning interactions among species of cleaner gobies Tigrigobius spp. and Elacatinus puncticulatus (family Gobiidae) and the client fish species they clean in a coral reef of Gorgona Island, Colombia. In 419 cleaning events, we observed 27 species acting as clients of Tigrigobius spp., whereas only nine were clients of E. puncticulatus. Paranthias colonus and Cephalopholis panamensis were the species most commonly cleaned by Tigrigobius spp., while Ophioblennius steindachneri and Stegastes acalpulcoensis were the clients most commonly cleaned by E. puncticulatus. The abundance (but not the body size) of clients was an important variable predicting the cleaning frequency observed for clients of Tigrigobius spp., but this was not the case for clients of E. puncticulatus. Additionally, Tigrigobius spp. preferred cleaning planktivores, sessile invertebrate feeders and territorial herbivores (Ivlev's index >0·15), whereas E. puncticulatus did not exhibit any preference. We observed two major peaks of cleaning activity for Tigrigobius spp., one in the early morning and another one in the late afternoon. These results suggest that Tigrigobius spp. is a specialized cleaner goby, whereas E. puncticulatus is a facultative cleaner that cleans sporadically.     

To clean or not to clean: Cleaning mutualism breakdown in a tidal environment

The dynamics and prevalence of mutualistic interactions, which are responsible for the maintenance and structuring of all ecological communities, are vulnerable to changes in abiotic and biotic environmental conditions. Mutualistic outcomes can quickly shift from cooperation to conflict, but it unclear how resilient and stable mutualistic outcomes are to more variable conditions. Tidally controlled coral atoll lagoons that experience extreme diurnal environmental shifts thus provide a model from which to test plasticity in mutualistic behavior of dedicated (formerly obligate) cleaner fish, which acquire all their food resources through client interactions. Here, we investigated cleaning patterns of a model cleaner fish species, the bluestreak wrasse (Labroides dimidiatus), in an isolated tidal lagoon on the Great Barrier Reef. Under tidally restricted conditions, uniquely both adults and juveniles were part‐time facultative cleaners, pecking on Isopora palifera coral. The mutualism was not completely abandoned, with adults also wandering across the reef in search of clients, rather than waiting at fixed site cleaning stations, a behavior not yet observed at any other reef. Contrary to well‐established patterns for this cleaner, juveniles appeared to exploit the system, by biting (“cheating”) their clients more frequently than adults. We show for the first time, that within this variable tidal environment, where mutualistic cleaning might not represent a stable food source, the prevalence and dynamics of this mutualism may be breaking down (through increased cheating and partial abandonment). Environmental variability could thus reduce the pervasiveness of mutualisms within our ecosystems, ultimately reducing the stability of the system.     

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.     

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

Background

Marine 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.

Results

For 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.

Conclusion

It 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.     

Degrees of honesty: cleaning by the redlip cleaner wrasse Labroides rubrolabiatus

Cleaning symbioses among coral reef fishes are highly variable. Cleanerfishes vary in how much they cooperate with (i.e. remove only ectoparasites) or cheat (i.e. bite healthy tissue, scales or mucus) on their fish clients. As a result, clients use various strategies to enforce cooperation by cleaners (e.g. punishment or partner choice), and cleaners use tactile stimulation to manipulate cheated client behaviour. We provide the first detailed observations of cleaning behaviour of the redlip cleaner wrasse Labroides rubrolabiatus and ask where interactions with this cleanerfish lie on the continuum of cleanerfish honesty, client control, and cleanerfish manipulation. Ninety per cent of redlip cleaner wrasses took jolt-inducing cheating bites from their clients, but they did so at a very low rate (~ 2 jolts per 100 s inspection). Retaliatory chases by clients were uncommon. Three-quarters (30 of 40) of cleaner wrasses used tactile stimulation on their clients, but rarely did so to reconcile with cheated clients. Instead, the majority (70%) of tactile stimulation events targeted a passing client that then stopped for inspection. The relationship between redlip cleaner wrasses and their clients appears to be less conflictual than those documented in other Labroides cleanerfishes. Future studies should test whether this low level of conflict is consistent across space and time and is underpinned by a preference for ectoparasites over other client-gleaned items. As an active cleaner that appears to take few cheating bites from their clients, L. rubrolabiatus has the potential to be as important a driver of fish health and community structure on coral reefs as its better-known relatives.

     

Cleaner wrasse mimics inflict higher costs on their models when they are more aggressive towards signal receivers

Aggressive mimics are predatory species that resemble a 'model' species to gain access to food, mating opportunities or transportation at the expense of a signal receiver. Costs to the model may be variable, depending on the strength of the interaction between mimics and signal receivers. In the Indopacific, the bluestriped fangblenny Plagiotremus rhinorhynchos mimics juvenile cleaner wrasse Labroides dimidiatus. Instead of removing ectoparasites from larger coral reef fish, fangblennies attack fish to feed on scales and body tissue. In this study, juvenile cleaner wrasse suffered significant costs when associated with P. rhinorhynchos mimics in terms of reduced cleaning activity. Furthermore, the costs incurred by the model increased with heightened aggression by mimics towards signal receivers. This was apparently because of behavioural changes in signal receivers, as cleaning stations with mimics that attacked frequently were visited less. Variation in the costs incurred by the model may influence mimicry accuracy and avoidance learning by the signal receiver and thus affect the overall success and maintenance of the mimicry system.     

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.     

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.