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.     

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.     

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.     

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.     

Linking cranial morphology to prey capture kinematics in three cleaner wrasses: Labroides dimidiatus,Larabicus quadrilineatus,and Thalassoma lutescens

Cleaner fishes are well known for removing and consuming ectoparasites off other taxa. Observers have noted that cleaners continuously “pick” ectoparasites from the bodies of their respective client organisms, but little is known about the kinematics of cleaning. While a recent study described the jaw morphology of cleaners as having small jaw‐closing muscles and weak bite forces, it is unknown how these traits translate into jaw movements during feeding to capture and remove ectoparasites embedded in their clients. Here, we describe cranial morphology and kinematic patterns of feeding for three species of cleaner wrasses. Through high‐speed videography of cleaner fishes feeding in two experimental treatments, we document prey capture kinematic profiles for Labroides dimidiatus, Larabicus quadrilineatus, and Thalassoma lutescens. Our results indicate that cleaning in labrids may be associated with the ability to perform low‐displacement, fast jaw movements that allow for rapid and multiple gape cycles on individually targeted items. Finally, while the feeding kinematics of cleaners show notable similarities to those of “picker” cyprinodontiforms, we find key differences in the timing of events. In fact, cleaners generally seem to be able to capture prey twice as fast as cyprinodontiforms. We thus suggest that the kinematic patterns exhibited by cleaners are indicative of picking behavior, but that “pickers” may be more kinematically diverse than previously thought. J. Morphol. 276:1377–1391, 2015. © 2015 Wiley Periodicals, Inc.     

Variation in posing behaviour among fish species visiting cleaning stations

The adaptive significance of posing behaviour by fish visiting cleaning stations on a Barbadian fringing reef was investigated. The probability of a visitor being cleaned by cleaning gobies ( Elacatinus spp.) was significantly higher after posing than after failing to pose upon arrival at a cleaning station. Despite this, not all visitors posed, and there was much variation among species in tendency to pose. This interspecific variation was not related to the probability of being cleaned, either after posing or after failing to pose, nor was it related to trophic level or fish total length. The latter was true both for cross-species analyses and phylogenetically independent contrasts. A cost-benefit model is proposed to understand interspecific variation in posing behaviour, which considers both decisions by clients and by cleaners. As well as explaining the results, this may reconcile differences among anecdotal and experimental observations from previous studies.     

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.     

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 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.     

Up or down? Explaining the variability of communication signals in cleaning symbioses

In this study, we used cleaning symbioses among coral reef fishes as a model system to investigate the form and function of signalling in interspecific mutualisms. More specifically, we examined the causes and significance of inter‐specific and inter‐individual variation in the design of client solicitation poses in cleaning interactions with Caribbean cleaning gobies ( Elacatinus spp). Using empirical data collected during field observations at cleaning stations, we tested three hypotheses: (1) The form of client incitation poses depends on species‐specific features; (2) Intraspecific variability in the form of client poses reflects the strength of each cleaner‐client relationship; and (3) Client individuals that deviate from a clear species‐specific form of pose will receive a different cleaning service. As predicted by (1), we found that the type of incitation pose was related to client body size, with small species performing mainly head‐down displays which may facilitate retreat into coral cavities upon predator approach. There was nevertheless some intraspecific variation in the type of display performed by clients, which was negatively related to client ectoparasite load, as predicted by (2). Hence, species with higher ectoparasite loads, and thus with a greater need to be cleaned, were less variable in display form than clients with fewer ectoparasites. Finally, cleaning gobies inspected for longer those individual clients that performed the species‐specific solicitation poses (3). We conclude that solicitation poses function to minimize uncertainty about a client's need to be cleaned and that their design has been partly determined by the risk of predation on posing clients.     

Ectoparasites: are they the proximate cause of cleaning interactions?

We tested the importance of ectoparasites in cleaning symbioses 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 are inactive, than during the day. Overall ectoparasite loads also tended to be higher on clients in the morning. This coincided with higher rates of visits to cleaning stations by client fish in the morning than at midday, but high rates of client visits were also recorded in the late afternoon. Clients were more likely to adopt stereotypical incitation poses, which increase the likelihood of being cleaned, in the morning than later in the day. Inspection bouts by cleaning gobies were longest in the morning. Cleaner and client behaviours therefore change predictably in response to natural diurnal variation in ectoparasite availability. These results add to a growing number of studies supporting the idea that cleaning symbioses are mutualisms dependent on ectoparasite removal.     

Mutualism or parasitism? The variable outcome of cleaning symbioses

The exact nature of many interspecific interactions remains unclear, with some evidence suggesting mutualism and other evidence pointing to parasitism for the same pair of interacting species. Here, we show spatial variation in the outcome of the cleaning relationship between Caribbean cleaning gobies (Elacatinus evelynae) and longfin damselfish (Stegastes diencaeus) over the distribution range of these species, and link this variation to the availability of ectoparasites. Cleaning interactions at sites with more ectoparasites were characterized by greater reductions in ectoparasite loads on damselfish clients and lower rates of removal of scales and mucus (i.e. cheating) by cleaning gobies, whereas the opposite was observed at sites where ectoparasite abundance was lower. For damselfish clients, cleaning was therefore clearly mutualistic in some locations, but sometimes neutral or even parasitic in others. Seasonal variability in ectoparasite abundance may ensure that locally low parasite availability, which promotes cleanerfish cheating, may be a transient condition at any given site. Conflicting conclusions about the nature of cleaning symbioses may, therefore, be explained by variation in ectoparasite abundance.     

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.     

Evaluation of the effect of cleaning regimes on biofilms of thermophilic bacilli on stainless steel

AIMS: To determine the mechanism for both the removal and inactivation of 18-h biofilms of a thermophilic Bacillus species that optimally grows at 55 degrees C on stainless steel. METHODS AND RESULTS: The cleaning strategies tested were based on biofilm biochemistry and physiology, and focused on the chemistry of the cleaners, the duration and temperature of the cleaning process and a combination of various cleaners. The success of the cleaning regimes was determined based on the removal of cells and organic debris and the elimination of viable cells. The results confirmed that a caustic (75 degrees C for 30 min) and acid (75 degrees C for 30 min) wash, relied upon heavily in most food processing industries for cleaning-in-place systems, was successful in removing these biofilms. However, any changes in the concentrations of these cleaners or the temperature of cleaning drastically affected the overall outcome. Alternative cleaning agents based on enzymatic or nonenzymatic breakdown of cellular proteins or polysaccharides, surfactant action, use of oxidative attack and free radicals varied in degrees of their success. Combining proteolytic action with surfactants increased wetability and therefore enhanced the cleaning efficiency. CONCLUSIONS: Several procedures, including caustic/acid and enzyme based cleaners, will be satisfactory, provided that the correct process parameters are observed i.e. concentration, time, temperature and kinetic energy (flow). Confirmation of these results should be carried out in a pilot plant through several use/clean cycles. SIGNIFICANCE AND IMPACT OF THE STUDY: Confidence in standard and alternative cleaning procedures for food manufacturing plant to prevent contamination with thermophilic bacilli that threaten product quality.     

Cleaning behavior is riskier and less profitable than an alternative strategy for a facultative cleaner fish

Cleaning symbioses on coral reefs involve small cleaner fish or shrimps picking ectoparasites from the exterior surfaces of larger client organisms. These mutualisms are thought to evolve in part because the cleaner receives a reliable source of profitable prey items and immunity from predation. However, the benefits of cleaning behavior have never been measured relative to those of alternative, non-cleaning strategies. This study examined these costs and benefits in the sharknose goby, Elacatinus evelynae, a facultative cleaner fish, at the Caribbean island of St. Croix. Sharknose gobies are found on coral heads, where they maintain cleaning stations, and on basket sponges, where they spend little time cleaning and feed predominantly on nonparasitic copepods. For immature gobies that are not allocating energy to reproduction, hindcast otolith growth rates (a reliable proxy for somatic growth) were significantly higher for non-cleaning sponge-dwellers than for coral-dwellers. Furthermore, tagging large, competitively dominant gobies on sponges and corals revealed that mortality rates were higher for coral-dwelling gobies. These unexpected results provide further evidence that cleaning mutualisms are context dependent: far from being a uniformly profitable life history strategy, cleaning may be a suboptimal choice at some times and places.     

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.     

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.     

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.     

Co-evolution of cleaning and feeding morphology in western Atlantic and eastern Pacific gobies

Cleaning symbioses are mutualistic relationships where cleaners remove and consume ectoparasites from their clients. Cleaning behavior is rare in fishes and is a highly specialized feeding strategy only observed in around 200 species. Cleaner fishes vary in their degree of specialization, ranging from species that clean as juveniles or facultatively as adults, to nearly obligate or dedicated cleaners. Here, we investigate whether these different levels of trophic specialization correspond with similar changes in feeding morphology. Specifically, we model the evolution of cleaning behavior across the family Gobiidae, which contains the most speciose radiation of dedicated and facultative cleaner fishes. We compared the cranial morphology and dentition of cleaners and non-cleaners across the phylogeny of cleaning gobies and found that facultative cleaners independently evolved four times and have converged on an intermediate morphology relative to that of dedicated cleaners and non-cleaning generalists. This is consistent with their more flexible feeding habits. Cleaner gobies also possess a distinct tooth morphology, which suggests they are adapted for scraping parasites off their clients and show little similarity to other cleaner clades. We propose that evolutionary history and pre-adaptation underlie the morphological and ecological diversification of cleaner fishes.     

Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs

Mutualisms affect the biodiversity, distribution and abundance of biological communities. However, ecological processes that drive mutualism-related shifts in population structure are often unclear and must be examined to elucidate how complex, multi-species mutualistic networks are formed and structured. In this study, we investigated how the presence of key marine mutualistic partners can drive the organisation of local communities on coral reefs. The cleaner wrasse, Labroides dimidiatus, removes ectoparasites and reduces stress hormones for multiple reef fish species, and their presence on coral reefs increases fish abundance and diversity. Such changes in population structure could be driven by increased recruitment of larval fish at settlement, or by post-settlement processes such as modified levels of migration or predation. We conducted a controlled field experiment to examine the effect of cleaners on recruitment processes of a common group of reef fishes, and showed that small patch reefs (61–285 m²) with cleaner wrasse had higher abundances of damselfish recruits than reefs from which cleaner wrasse had been removed over a 12-year period. However, the presence of cleaner wrasse did not affect species diversity of damselfish recruits. Our study provides evidence of the ecological processes that underpin changes in local population structure in the presence of a key mutualistic partner.