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.     

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.     

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.     

Size-selective predation by the cleaner fish Labroides dimidiatus

A comparison of the size-frequency distribution of parasitic gnathiid isopod larvae in the diet of the cleaner fish Labroides dimidiatus and on six host fish species ( Chlorurus sordidus, Ctenochaetus striatus, Hemigymnus melapterus, Scolopsis bilineatus, Siganus doliatus, Thalassoma lunare ) was made on one occasion. The comparison was repeated with Hemigymnus melapterus on three occasions and between two islands in Australia. L. dimidiatus selected larger gnathiids at all times at Lizard Island but not at Heron Island. Size-selective predation by L. dimidiatus suggests any potential effect of cleaner fish on parasites may vary according to the size of parasite. However, this effect appears to vary spatially.     

Reversed Sex-Change in the Protogynous Reef Fish Labroides dimidiatus

Protogynous hermaphroditism, or female-to-male sex change, is known for many reef fishes including wrasses (family Labridae) in which large males monopolize mating. When the dominant male disappears from a polygynous group, the largest female may change sex within a few weeks. Such social control of sex change was first documented in harems of the cleaner wrasse Labroides dimidiatus almost 30 yr ago. To examine whether change of social status would induce males of L. dimidiatus to perform reversed sex-change, we conducted experiments: (i) releasing single males near lone males whose mates have been removed in the field; and (ii) keeping two males in a tank. Smaller males changed back to females when they became subordinate: it took 53–77 d (n=3) for them to complete gonadal sex change and release eggs in the aquarium. The male–male pairs performed spawning behavior, with the smaller male in the female role already 5–58 d before completion of gonadal sex change. This is the first report of reversed sex-change among protogynous wrasses. Moreover, we conducted another experiment, keeping a pair of a male and a larger female in a tank (n=1). We found sex change by both mates, which has not been reported from any fishes. Thus, the sex of L. dimidiatus is strictly determined by social status whenever it changes after mate loss.     

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.     

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.     

Short‐Term Variation in the Level of Cooperation in the Cleaner Wrasse Labroides dimidiatus: Implications for the Role of Potential Stressors

There is a wealth of game theoretical approaches to the evolution and maintenance of cooperation between unrelated individuals and accumulating empirical tests of these models. This contrasts strongly with our lack of knowledge on proximate causes of cooperative behaviour. Marine cleaning mutualism has been used as a model system to address functional aspects of conflict resolution: client reef fish benefit from cleaning interactions through parasite removal, but cleaner fish Labroides dimidiatus prefer client mucus. Hence, feeding against their preference represents cooperative behaviour in cleaners. Cleaners regularly cheat non‐predatory clients while they rarely cheat predatory clients. Here, we asked how precisely cleaners can adjust service quality from one interaction to the next. We found that non‐predatory clients receive a better service if the previous client was a predator than if the previous client was a non‐predator. In a related laboratory experiment, a hand‐net used as a stressor resulted in cleaners feeding more against their preference in subsequent interactions. The combination of the cleaners’ behaviour in the two studies shows that the cleaners’ service quality for a given client species is not fixed, but it can be manipulated. The results suggest that short‐term stress is one factor that causes cleaners to increase their levels of cooperation, a hypothesis that is amenable to further experiments manipulating the endocrine system.     

Long-term effects of the cleaner fish Labroides dimidiatus on coral reef fish communities

Cleaning behaviour is deemed a mutualism, however the benefit of cleaning interactions to client individuals is unknown. Furthermore, mechanisms that may shift fish community structure in the presence of cleaning organisms are unclear. Here we show that on patch reefs (61–285 m²) which had all cleaner wrasse Labroides dimidiatus (Labridae) experimentally removed (1–5 adults reef⁻¹) and which were then maintained cleaner-fish free over 8.5 years, individuals of two site-attached (resident) client damselfishes (Pomacentridae) were smaller compared to those on control reefs. Furthermore, resident fishes were 37% less abundant and 23% less species rich per reef, compared to control reefs. Such changes in site-attached fish may reflect lower fish growth rates and/or survivorship. Additionally, juveniles of visitors (fish likely to move between reefs) were 65% less abundant on removal reefs suggesting cleaners may also affect recruitment. This may, in part, explain the 23% lower abundance and 33% lower species richness of visitor fishes, and 66% lower abundance of visitor herbivores (Acanthuridae) on removal reefs that we also observed. This is the first study to demonstrate a benefit of cleaning behaviour to client individuals, in the form of increased size, and to elucidate potential mechanisms leading to community-wide effects on the fish population. Many of the fish groups affected may also indirectly affect other reef organisms, thus further impacting the reef community. The large-scale effect of the presence of the relatively small and uncommon fish, Labroides dimidiadus, on other fishes is unparalleled on coral reefs.     

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

Memory 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.     

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.     

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.     

Spawning timing of the cleaner wrasse, Labroides dimidiatus, on a warm temperate rocky shore

We observed spawning behaviors of the haremic cleaner wrasse Labroides dimidiatus at a rocky reef in southern Japan. Females released pelagic eggs daily from June to September after a spawning ascent by pairs. When the high tide occurred between noon and evening (quarter moon to new or full moon), they spawned around the time of the tide providing fast offshore currents. For the rest of the lunar cycle, spawnings occurred during late afternoon independent of the state of the tide at the time of day. This spawning pattern is quite different from that of conspecifics on coral reefs that always spawn around the high tide at all lunar stages to avoid potential egg predators. The wrasse ascended high in the water column, probably because of its predator-immune characters as a cleaner. The steep slope of the study site seemed to contribute to releasing gametes far above aggregating planktivores. Thus, gametes were not subject to heavy predation. Current direction might not always affect survival of spawned pelagic eggs on the temperate reefs so crucially as it does on coral reefs. We conclude that spawning during unfavorable tidal conditions during the daytime may be better than spawning during the best tidal condition in the crepuscular period when predation pressure on adults will be high. Intraspecific variation in the timing and location of spawning of the wrasse may result from different conditions for larval survival. Received: February 6, 2000 / Revised: June 16, 2000 / Accepted: July 17, 2000     

The effect of the cleaner fish Labroides dimidiatus on the capsalid monogenean Benedenia lolo parasite of the labrid fish Hemigymnus melapterus

The cleaner fish Labroides dimidiatus affected the pigmented monogenean parasite Benedenia lolo on the fish Hemigymnus melapterus (Labridae) held in aquaria. The effect of cleaner fish varied with the size class of fish; only small fish [ a posteriori size class <11.5 cm standard length ( L _S)] exposed to cleaner fish had fewer monogeneans compared with fish not exposed to cleaner fish. The abundance of monogeneans on large fish ( a posteriori size class <11.5 cm L _S) was not affected by cleaner fish. The size-frequency distributions of monogeneans on both size-classes of H. melapterus were affected by cleaner fish. Fish exposed to cleaner fish had fewer large (>3 mm) and more small (<1 mm) monogeneans than fish not exposed to cleaner fish, suggesting cleaner fish selectively removed larger monogeneans. This difference was more pronounced on large fish. In the absence of cleaner fish, small fish had almost as many monogeneans as large fish; they also had more small monogeneans than the large fish, suggesting small fish were more vulnerable to infection by monogeneans than larger fish. This suggests that the cleaner fish L. dimidiatus has the potential to control benedeniine monogeneans on captive fish and highlights the importance of taking into account fish size in studies of the effect of cleaner fish on ectoparasites.     

Chimpanzees are more skilful in competitive than in cooperative cognitive tasks

In a series of four experiments, chimpanzees, Pan troglodytes, were given two cognitive tasks, an object choice task and a discrimination task (based on location), each in the context of either cooperation or competition. In both tasks chimpanzees performed more skilfully when competing than when cooperating, with some evidence that competition with conspecifics was especially facilitatory in the discrimination location task. This is the first study to demonstrate a facilitative cognitive effect for competition in a single experimental paradigm. We suggest that chimpanzee cognitive evolution is best understood in its socioecological context.     

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.     

The opercular gland of the cleaner-wrasse Labroides dimidiatus (Labridae), a light-, electron and scanning electron microscopic investigation

A histological and ultrastructural examination of the opercular gland of the cleaner-wrasse Labroides dimidiutus has demonstrated that the slimy envelope which covers the animal at night is mainly produced by large mucous goblet cells in a folded epithelium; there is a high number of acidophilic secretory cells. At the ultrastructural level, both cell-types open at the surface of the epidermis. Preliminary experiments with pilocarpine, atropine and the α-blocker propranolol reveal a neural regulation of mucus discharge. Also, the rich vascularization of the gland could indicate a hormonal control e.g. by prolactin. The secretory products of both types of goblet cells are discussed in relation to their possible antibiotic properties.     

The effects of competition and the presence of an audience on weight lifting performance

The purpose of this investigation was to examine the effects of the presence of an audience and competition on maximal weight lifting performance. Thirty-two recreationally trained participants (15 men, 17 women; 21 +/- 2.5 years) performed a 1 repetition maximum (1 RM) bench press during 3 different situations (coaction, competitive coaction, and audience condition). Subjects also completed the Activation-Deactivation Adjective Checklist Short Form following the 3 trials to measure arousal state during each of the 3 trials. Significant differences (p < 0.05) were found between competitive coaction and coaction trials as well as between audience and coaction trials. Both men and women demonstrated the highest performance in front of an audience (105 +/- 48 kg) followed by competition (103 +/- 46 kg) and then the coaction trial (93 +/- 43 kg). No significant difference in arousal was measured between trials. The data suggest that performing a maximal lift in the presence of an audience or in competition facilitates performance and support the self-presentation and self-awareness theories. Social facilitation effects should be controlled in research settings and may aid the performance of weight lifting activities during events or competition.     

The presence of an avian co-forager reduces vigilance in a cooperative mammal

Many animals must trade-off anti-predator vigilance with other behaviours. Some species facilitate predator detection by joining mixed-species foraging parties and ‘eavesdropping’ on the predator warnings given by other taxa. Such use of heterospecific warnings presumably reduces the likelihood of predation, but it is unclear whether it also provides wider benefits, by allowing individuals to reduce their own vigilance. We examine whether the presence of an avian co-forager, the fork-tailed drongo (Dicrurus adsimilis), affects rates of vigilance (including sentinel behaviour) in wild dwarf mongooses (Helogale parvula). We simulate the presence of drongos—using playbacks of their non-alarm vocalizations—to show that dwarf mongooses significantly reduce their rate of vigilance when foraging with this species. This is, to our knowledge, the first study to demonstrate experimentally that a mammal reduces vigilance in the presence of an avian co-forager.