Reexamination on the aggressive mimicry of the cleaner wrasseLabroides dimidiatus by the blennyAspidontus taeniatus (Pisces; Perciformes)

Field observations on feeding and related behavior of the mimic blennyAspidontus taeniatus and 3 species closely related to it, and the cleaner fish (model)Labroides dimidiatus were made at the coral reef of Sesoko Island, Okinawa, Japan, along with analysis of gut contents. The mimic blenny fed mostly on demersal eggs of fishes and tentacles of polychaetes, but it rarely tore pieces from the fins of host fishes even when they were posing for cleaning. The feeding habits of the mimic blenny are compared with those in other localities and with those of related species. It is concluded that the mimicry can hardly be regarded as an aggressive one: posing by host fishes seems to be a secondary result of the resemblance which may have developed because of the benefit for immunity from predation, and the resemblance itself prevents the blenny from becoming a specialized fin-eater because it can be easily recognized by host fishes.     

Experimental confirmation of aggressive mimicry by a coral reef fish

A number of potential mimetic relationships between coral reef fishes have been described, but the underlying mechanisms are poorly understood. Similarities in colour between species have often been attributed to aggressive mimicry (where predators resemble models in order to deceive prey), however this has not been tested. The fang blenny, Plagiotremus rhinorhynchos is a specialized predator that feeds on tissues of other fishes. Some individuals appear to mimic the harmless cleaner wrasse Labroides dimidiatus in order to deceive fish visiting cleaning stations, thereby increasing access to food. In this study, the ecological relationship between the mimic and model was examined at Kimbe Bay (Papua New Guinea) and the hypothesis that colour similarities represent facultative aggressive mimicry was experimentally evaluated. Some juveniles exhibited a striking resemblance to the juvenile colouration of the cleaner wrasse, but only when in close proximity to the wrasse and only when similar in size. As predicted for mimics, P. rhinorhynchos co-occurred with L. dimidiatus, but was rare relative to the model. Among site comparisons showed that the abundance of mimetic type blennies was positively correlated with the abundance of juvenile cleaner wrasses. Approximately 50% of all P. rhinorhynchos were found 1 m from the nearest L. dimidiatus, a distance significantly shorter than expected if they were not associated. A cleaner wrasse removal experiment was carried out to test whether the colour displayed by the blenny and its foraging success were contingent upon the presence of a model. In all cases, removal of the model prompted a rapid colour change to a general non-mimetic colouration in P. rhinorhynchos. Removal of L. dimidiatus also resulted in a ~20% reduction in the average foraging success of the blenny compared to controls, supporting the hypothesis that the blenny is a facultative aggressive mimic of the cleaner wrasse.     

Effects of group behavior in the predatory raid on damselfish nests by the false cleanerfish Aspidontus taeniatus

The false cleanerfish Aspidontus taeniatus, which resembles the bluestreak cleaner wrasse Labroides dimidiatus, is one of the best-known examples of mimicry in vertebrates. This mimicry system has been viewed as an aggressive mimicry to bite fish fins. However, recent field studies have reported that large individuals of the false cleanerfish often form groups and jointly raid damselfish nests to eat eggs that are guarded by their parents. The benefits of group behavior have been reported in a variety of animals. In the case of false cleanerfish, parental defense of territorial damselfishes is the main factor that constrains the availability of nutritionally valuable food resources. Here, we conducted field observations on the reefs of Okinawa, and found that the false cleanerfish formed groups of 2–12 individuals when they raided breeding nests of 13 species of damselfishes (Pomacentridae) and one species of triggerfish (Balistidae). Since the cleaner wrasse does not form such groups, the feeding groups of the false cleanerfish are assumed to reduce the effectiveness of mimicry. However, our results showed that the group behavior has two effects: a dilution effect, which reduces the risk of being attacked by egg-guarding fish, and an increase in foraging efficiency. We conclude that the false cleanerfish need to form foraging groups during egg-eating because the mimicry has no effect on parental damselfishes.     

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.     

A protective function for aggressive mimicry?

Mimicry often involves a protective element, whereby the risk of predation on mimics is reduced owing to their resemblance to unpalatable models. However, protection from predation has so far seemed unimportant in aggressive mimicry, where mimics are usually predators rather than prey. Here, we demonstrate that bluestriped fangblennies (Plagiotremus rhinorhynchos), which are aggressive mimics of juvenile bluestreak cleaner wrasse (Labroides dimidiatus), derive significant protection benefits from their resemblance to cleaner fish. Field observations revealed that mimetic fangblennies were chased by potential victims less often than individuals of a closely related, ecologically and behaviourally similar but non-mimetic species (Plagiotremus tapeinosoma). After attacks, proximity to models protected mimics from retaliation by victims, but the effect of colour similarity was less clear. Both colour resemblance and physical proximity to models thus appear to protect cleaner-fish mimics from aggression by potential and actual victims of their attacks. Our results suggest that the mimicry types observed in nature, which are usually distinguished on the basis of the benefits accrued to mimics, may in fact overlap greatly in the benefits provided.     

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.     

Facultative mimicry: cues for colour change and colour accuracy in a coral reef fish

Mimetic species evolve colours and body patterns to closely resemble poisonous species and thus avoid predation (Batesian mimicry), or resemble beneficial or harmless species in order to approach and attack prey (aggressive mimicry). Facultative mimicry, the ability to switch between mimic and non-mimic colours at will, is uncommon in the animal kingdom, but has been shown in a cephalopod, and recently in a marine fish, the bluestriped fangblenny Plagiotremus rhinorhynchos, an aggressive mimic of the juvenile cleaner fish Labroides dimidiatus. Here we demonstrate for the first time that fangblennies adopted mimic colours in the presence of juvenile cleaner fish; however, this only occurred in smaller individuals. Field data indicated that when juvenile cleaner fish were abundant, the proportion of mimic to non-mimic fangblennies was greater, suggesting that fangblennies adopt their mimic disguise depending on the availability of cleaner fish. Finally, measurements of spectral reflectance suggest that not only do mimic fangblennies accurately resemble the colour of their cleaner fish models but also mimic other species of fish that they associate with. This study provides insights into the cues that control this remarkable facultative mimicry system and qualitatively measures its accuracy.     

Distance-dependent costs and benefits of aggressive mimicry in a cleaning symbiosis

In aggressive mimicry, a 'predatory' species resembles a model that is harmless or beneficial to a third species, the 'dupe'. We tested critical predictions of Batesian mimicry models, i.e. that benefits of mimicry to mimics and costs of mimicry to models should be experienced only when model and mimic co-occur, in an aggressive mimicry system involving juvenile bluestreaked cleaner wrasse (Labroides dimidiatus) as models and bluestriped fangblennies (Plagiotremus rhinorhynchos) as mimics. Cleanerfish mimics encountered nearly twice as many potential victims and had higher striking rates when in proximity to than when away from the model. Conversely, in the presence of mimics, juvenile cleaner wrasses were visited by fewer clients and spent significantly less time foraging. The benefits to mimic and costs to model thus depend on a close spatial association between model and mimic. Batesian mimicry theory may therefore provide a useful initial framework to understand aggressive mimicry.     

Patterns of Local Distribution of Labroides Dimidiatus in French Polynesian Atolls

Cleaning behaviour by fishes has been described to be either facultative or specialised. If being specialised in cleaning is more advantageous than to be a facultative cleaner, cleaner fishes would prefer to settle on reefs were ecological conditions promote specialisation. To test this hypothesis, we looked at the influence of physical and ecological factors on cleaner wrasse abundance, studying variations in L. dimidiatus density between 10 atolls of French Polynesia. We used a multiple regression method based on permutations of distance matrices. Our study reveals that L. dimidiatus are significantly more numerous at sites where ecological factors, such as the species richness of the fish community, may promote their cleaning activity. Moreover, they were significantly more abundant in atolls presenting a large number of sedentary fish species, few predators and few fishes living in large groups. Finally, physical factors, such as the distance between atolls, the lagoon surface, the mean percentage of hard substrate, the mean current index, and the mean depth, play a minor role in the occurrence of L. dimidiatus.     

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.     

Comparison of mortality and feeding behavior of the false cleanerfish Aspidontus taeniatus and the lance blenny A. dussumieri regarding the effects of mimicry

Journal of Ethology - Many examples of mimicry have been reported in coral reef fishes of which the most well known is the mimicry of the bluestreak cleaner wrasse, Labroides dimidiatus by the...     

Aggressive mimics profit from a model-signal receiver mutualism

Mimetic species have evolved to resemble other species to avoid predation (protective mimicry) or gain access to food (aggressive mimicry). Mimicry systems are frequently tripartite interactions involving a mimic, model and 'signal receiver'. Changes in the strength of the relationship between model and signal receiver, owing to shifting environmental conditions, for example, can affect the success of mimics in protective mimicry systems. Here, we show that an experimentally induced shift in the strength of the relationship between a model (bluestreak cleaner fish, Labroides dimidiatus) and a signal receiver (staghorn damselfish, Amblyglyphidodon curacao) resulted in increased foraging success for an aggressive mimic (bluestriped fangblenny, Plagiotremus rhinorhynchos). When the parasite loads of staghorn damselfish clients were experimentally increased, the attack success of bluestriped fangblenny on damselfish also increased. Enhanced mimic success appeared to be due to relaxation of vigilance by parasitized clients, which sought cleaners more eagerly and had lower overall aggression levels. Signal receivers may therefore be more tolerant of and/or more vulnerable to attacks from aggressive mimics when the net benefit of interacting with their models is high. Changes in environmental conditions that cause shifts in the net benefits accrued by models and signal receivers may have important implications for the persistence of aggressive mimicry systems.     

Predators favour mimicry in a tropical reef fish

Batesian mimicry evolves when the 'umbrella' of protection provided by resemblance to a conspicuous unpalatable model species is sufficient to overcome increased predation risk associated with greater conspicuousness. However, the shape and extent of this umbrella, that is, how the level of protection provided by mimicry changes with degree of resemblance between model and mimic, is poorly known. We investigated the response of wild predatory fishes to plastic replicas of a model-mimic species pair of tropical reef fishes, Canthigaster valentini (a toxic pufferfish, the model) and Paraluteres prionurus (the putative mimic), and additional replicas with progressively lower degrees of resemblance to the mimic species. Our results reveal a relatively broad region of protection, indicated by a reduced approach rate by piscivorous fishes, surrounding the colour pattern of the model species. Protection increased with increasing resemblance. By contrast, the response of non-piscivorous fishes was unrelated to degree of resemblance of replicas to the model. Our results suggest that piscivorous fishes on the reef are educated regarding the toxicity of C. valentini, and that avoidance of fish having the pufferfish colour pattern has generated selection favouring mimetic resemblance by the palatable P. prionurus. The relatively broad protective umbrella has probably facilitated the initial evolution of resemblance in the palatable prey species despite the potential hazards of greater conspicuousness.     

Fish-egg predation by the small clingfish <Emphasis Type="Italic">Pherallodichthys meshimaensis</Emphasis>(Gobiesocidae) on the shallow reefs of Kuchierabu-jima Island,southern Japan

Synopsis We observed predation of demersal fish eggs by the clingfish Pherallodichthys meshimaensis on the shallow reefs of Kuchierabu-jima Island, southern Japan. The processes of egg predation varied with the target species. For targeting of eggs of the combtooth blenny Istiblennius edentulus, up to 65 individuals of the clingfish gathered around the I. edentulus nest hole. Some individuals succeeded in intruding into the hole and fed on eggs while the egg-guarding male of I. edentulus temporarily left the nest. For targeting of eggs of the triplefin blenny Helcogramma obtusirostris, solitary clingfish individuals closely approached spawning females of H. obtusirostris at nests on open surfaces of rocks. Most clingfish contained only fish eggs in their diets, and these fish-egg eaters had larger body sizes than individuals that mainly fed on harpacticoid crustacea. Thus, P. meshimaensis may change its feeding habits when growing to an obligate fish-egg eater targeting demersal egg spawners.     

Egg shape mimicry in parasitic cuckoos

Parasitic cuckoos lay their eggs in nests of host species. Rejection of cuckoo eggs by hosts has led to the evolution of egg mimicry by cuckoos, whereby their eggs mimic the colour and pattern of their host eggs to avoid egg recognition and rejection. There is also evidence of mimicry in egg size in some cuckoo–host systems, but currently it is unknown whether cuckoos can also mimic the egg shape of their hosts. In this study, we test whether there is evidence of mimicry in egg form (shape and size) in three species of Australian cuckoos: the fan‐tailed cuckoo Cacomantis flabelliformis, which exploits dome nesting hosts, the brush cuckoo Cacomantis variolosus, which exploits both dome and cup nesting hosts, and the pallid cuckoo Cuculus pallidus, which exploits cup nesting hosts. We found evidence of size mimicry and, for the first time, evidence of egg shape mimicry in two Australian cuckoo species (pallid cuckoo and brush cuckoo). Moreover, cuckoo–host egg similarity was higher for hosts with open nests than for hosts with closed nests. This finding fits well with theory, as it has been suggested that hosts with closed nests have more difficulty recognizing parasitic eggs than open nests, have lower rejection rates and thus exert lower selection for mimicry in cuckoos. This is the first evidence of mimicry in egg shape in a cuckoo–host system, suggesting that mimicry at different levels (size, shape, colour pattern) is evolving in concert. We also confirm the existence of egg size mimicry in cuckoo–host systems.     

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.     

Frequency-dependent success of aggressive mimics in a cleaning symbiosis

Batesian mimics-palatable organisms that resemble unpalatable ones-are usually maintained in populations by frequency-dependent selection. We tested whether this mechanism was also responsible for the maintenance of aggressive mimicry in natural populations of coral reef fishes. The attack success of bluestriped fangblennies (Plagiotremus rhinorhynchos), which mimic juvenile bluestreaked cleaner wrasses (Labroides dimidiatus) in colour but tear flesh and scales from fishes instead of removing ectoparasites, was frequency-dependent, increasing as mimics became rarer relative to their model. However, cleaner mimics were also more successful on reefs with higher densities of potential victims, perhaps because a dilution-like effect creates few opportunities for potential victims to learn to avoid mimics. Further studies should reveal whether this second mechanism is specific to aggressive mimicry.     

Who Resembles Whom? Mimetic and Coincidental Look-Alikes among Tropical Reef Fishes

Studies of mimicry among tropical reef-fishes usually give little or no consideration to alternative explanations for behavioral associations between unrelated, look-alike species that benefit the supposed mimic. I propose and assess such an alternative explanation. With mimicry the mimic resembles its model, evolved to do so in response to selection by the mimicry target, and gains evolved benefits from that resemblance. In the alternative, the social-trap hypothesis, a coincidental resemblance of the model to the “mimic” inadvertently attracts the latter to it, and reinforcement of this social trapping by learned benefits leads to the “mimic” regularly associating with the model. I examine three well known cases of supposed aggressive mimicry among reef-fishes in relation to nine predictions from these hypotheses, and assess which hypothesis offers a better explanation for each. One case, involving precise and complex morphological and behavioral resemblance, is strongly consistent with mimicry, one is inconclusive, and one is more consistent with a social-trap based on coincidental, imprecise resemblance. Few cases of supposed interspecific mimicry among tropical reef fishes have been examined in depth, and many such associations may involve social traps arising from generalized, coincidental resemblance. Mimicry may be much less common among these fishes than is generally thought.     

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

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

Cleaner wrasse influence habitat selection of young damselfish

The presence of bluestreak cleaner wrasse, Labroides dimidiatus, on coral reefs increases total abundance and biodiversity of reef fishes. The mechanism(s) that cause such shifts in population structure are unclear, but it is possible that young fish preferentially settle into microhabitats where cleaner wrasse are present. As a first step to investigate this possibility, we conducted aquarium experiments to examine whether settlement-stage and young juveniles of ambon damselfish, Pomacentrus amboinensis, selected a microhabitat near a cleaner wrasse (adult or juvenile). Both settlement-stage (0 d post-settlement) and juvenile (~5 weeks post-settlement) fish spent a greater proportion of time in a microhabitat adjacent to L. dimidiatus than in one next to a control fish (a non-cleaner wrasse, Halichoeres melanurus) or one where no fish was present. This suggests that cleaner wrasse may serve as a positive cue during microhabitat selection. We also conducted focal observations of cleaner wrasse and counts of nearby damselfishes (1 m radius) to examine whether newly settled fish obtained direct benefits, in the form of cleaning services, from being near a cleaner wrasse. Although abundant, newly settled recruits (<20 mm total length) were rarely (2 %) observed being cleaned in 20 min observations compared with larger damselfishes (58 %). Individual damselfish that were cleaned were significantly larger than the median size of the surrounding nearby non-cleaned conspecifics; this was consistent across four species. The selection by settlement-stage fish of a microhabitat adjacent to cleaner wrasse in the laboratory, despite only being rarely cleaned in the natural environment, suggests that even rare cleaning events and/or indirect benefits may drive their settlement choices. This behaviour may also explain the decreased abundance of young fishes on reefs from which cleaner wrasse had been experimentally removed. This study reinforces the potentially important role of mutualism during the processes of settlement and recruitment of young reef fishes.