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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Aggressive mimicry of the cleaner wrasse by Aspidontus taeniatus functions mainly for small blennies

The mimic blenny Aspidontus taeniatus Quoy & Gaimard is well known for its resemblance to the juvenile and adult cleaner wrasse Labroides dimidiatus (Valenciennes) in colour and shape. As various reef fishes including piscivores actively approach the cleaner wrasse to solicit cleaning by posing, two types of benefits have been suggested for this resemblance, that is, protective mimicry and aggressive mimicry. In aggressive mimicry, the mimic blenny is supposed to have considerable opportunities to bite the fin of deceived fishes when they pose, but some studies have confirmed that fin biting does not seem to be the main feeding tactic in the blenny in nature. Here, we examined the feeding tactics including fin biting by the mimic blenny in relation to its body size in a field observational survey in the coral reefs of Sesoko Island, Okinawa, Japan. The blenny was observed feeding mainly on four food items: the tentacles of Christmas tree worms, the mantle edges of boring clams, the demersal eggs in damselfishes’ nests and the fins of fishes. The feeding frequency by fin biting significantly decreased with body size, while that by egg predation significantly increased with body size of the blenny. When predating on eggs, the blenny was vigorously attacked by egg‐guarding fish, but often succeeded in raiding their nests by forming a feeding group. When feeding by fin biting, the blenny attacked prey fish without performing any cleaning. The ratio of fin biting was considerably higher in small‐sized blennies, suggesting reliance on this feeding tactic because of a difficulty in conducting a risky egg predation. Thus, our results suggest that the mimic blenny utilizes aggressive mimicry only when it is small as an alternative feeding tactic.     

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.     

Mimikry als Strategie von Jungfischen

Mimicry – a survival strategy for juvenile wrasses Due to high density of predators and competitors in coral reefs, especially juvenile fishes are forced to develop new survival strategies. In mimicry one animal shows great similarity to another in order to deceive its enemies. Juveniles of the wrasse genus Coris mimic the colouration of Anemone fish. Anemone fish live in symbiosis with their stinging host anemone and are therefore protected from predators. Wrasse mimics deceive their predators with their Anemone fish coloration in order to profit from higher survival rates.     

When more is less: the fitness consequences of predators attacking more unpalatable prey when more are presented

In 1879, Fritz Müller hypothesized that mimetic resemblance in which defended prey display the same warning signal would share the costs of predator education. Although Müller argued that predators would need to ingest a fixed number of prey with a given visual signal when learning to avoid unpalatable prey, this assumption lacks empirical support. We report an experiment which shows that, as the number of unpalatable prey presented to them increased, avian predators attacked higher numbers of those prey. We calculated that, when predators increase attacks, the fitness costs incurred by unpalatable prey can be substantial. This suggests that the survival benefits of mimicry could be lower than Müller proposed. An important finding is, however, that these costs decline in importance as the total number of available prey increases.     

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.     

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.     

Frequency-dependent variation in mimetic fidelity in an intraspecific mimicry system

Contemporary theory predicts that the degree of mimetic similarity of mimics towards their model should increase as the mimic/model ratio increases. Thus, when the mimic/model ratio is high, then the mimic has to resemble the model very closely to still gain protection from the signal receiver. To date, empirical evidence of this effect is limited to a single example where mimicry occurs between species. Here, for the first time, we test whether mimetic fidelity varies with mimic/model ratios in an intraspecific mimicry system, in which signal receivers are the same species as the mimics and models. To this end, we studied a polymorphic damselfly with a single male phenotype and two female morphs, in which one morph resembles the male phenotype while the other does not. Phenotypic similarity of males to both female morphs was quantified using morphometric data for multiple populations with varying mimic/model ratios repeated over a 3 year period. Our results demonstrate that male-like females were overall closer in size to males than the other female morph. Furthermore, the extent of morphological similarity between male-like females and males, measured as Mahalanobis distances, was frequency-dependent in the direction predicted. Hence, this study provides direct quantitative support for the prediction that the mimetic similarity of mimics to their models increases as the mimic/model ratio increases. We suggest that the phenomenon may be widespread in a range of mimicry systems.     

Cleaner shrimp use a rocking dance to advertise cleaning service to clients

Signals transmit information to receivers about sender attributes, increase the fitness of both parties, and are selected for in cooperative interactions between species to reduce conflict [1, 2]. Marine cleaning interactions are known for stereotyped behaviors [3-6] that likely serve as signals. For example, "dancing" and "tactile dancing" in cleaner fish may serve to advertise cleaning services to client fish [7] and manipulate client behavior [8], respectively. Cleaner shrimp clean fish [9], yet are cryptic in comparison to cleaner fish. Signals, therefore, are likely essential for cleaner shrimp to attract clients. Here, we show that the yellow-beaked cleaner shrimp [10] Urocaridella sp. c [11] uses a stereotypical side-to-side movement, or "rocking dance," while approaching potential client fish in the water column. This dance was followed by a cleaning interaction with the client 100% of the time. Hungry cleaner shrimp, which are more willing to clean than satiated ones [12], spent more time rocking and in closer proximity to clients Cephalopholis cyanostigma than satiated ones, and when given a choice, clients preferred hungry, rocking shrimp. The rocking dance therefore influenced client behavior and, thus, appears to function as a signal to advertise the presence of cleaner shrimp to potential clients.     

Juvenile Snooks (Centropomidae) as Mimics of Mojarras (Gerreidae), with a Review of Aggressive Mimicry in Fishes

Aggressive mimicry has been proposed for several unrelated fish species both in freshwater and marine environments. I describe herein a few additional examples, including the first ones from brackish water. In one well documented case, juvenile snooks, Centropomus mexicanus (Centropomidae) join bottom-foraging groups of the superficially similar mojarras, Eucinostomus melanopterus (Gerreidae) and prey on small fishes and crustaceans under such disguise. Two other snook species and two species of groupers (Serranidae), are here suggested as additional instances of aggressive mimicry. Furthermore, I review published examples of aggressive mimicry in fishes and indicate trends in the relationships between the mimics, their feeding tactics, and their putative models. Three large families, Serranidae, Cichlidae, and Blenniidae display most of the examples of aggressive mimicry, serranids being largely represented by the genus Hypoplectrus and blenniids by the tribe Nemophini only. Three major trends are here indicated for aggressive mimics: (1) fish species that feed on prey smaller than themselves tend to mimic and join fish species harmless to their prospective prey; (2) fish species that feed on prey larger than themselves tend to mimic mostly beneficial fish species (cleaners) or, less frequently, join species harmless to their prospective prey; (3) fish species that feed on prey about their own size tend to mimic their prospective prey species, the perfect wolf in a sheep's clothes disguise type. The latter deceit is recorded mostly for scale and fin-feeding freshwater fishes.     

Natural selection in mimicry

Biological mimicry has served as a salient example of natural selection for over a century, providing us with a dazzling array of very different examples across many unrelated taxa. We provide a conceptual framework that brings together apparently disparate examples of mimicry in a single model for the purpose of comparing how natural selection affects models, mimics and signal receivers across different interactions. We first analyse how model–mimic resemblance likely affects the fitness of models, mimics and receivers across diverse examples. These include classic Batesian and Müllerian butterfly systems, nectarless orchids that mimic Hymenoptera or nectar‐producing plants, caterpillars that mimic inert objects unlikely to be perceived as food, plants that mimic abiotic objects like carrion or dung and aggressive mimicry where predators mimic food items of their own prey. From this, we construct a conceptual framework of the selective forces that form the basis of all mimetic interactions. These interactions between models, mimics and receivers may follow four possible evolutionary pathways in terms of the direction of selection resulting from model–mimic resemblance. Two of these pathways correspond to the selective pressures associated with what is widely regarded as Batesian and Müllerian mimicry. The other two pathways suggest mimetic interactions underpinned by distinct selective pressures that have largely remained unrecognized. Each pathway is characterized by theoretical differences in how model–mimic resemblance influences the direction of selection acting on mimics, models and signal receivers, and the potential for consequent (co)evolutionary relationships between these three protagonists. The final part of this review describes how selective forces generated through model–mimic resemblance can be opposed by the basic ecology of interacting organisms and how those forces may affect the symmetry, strength and likelihood of (co)evolution between the three protagonists within the confines of the four broad evolutionary possibilities. We provide a clear and pragmatic visualization of selection pressures that portrays how different mimicry types may evolve. This conceptual framework provides clarity on how different selective forces acting on mimics, models and receivers are likely to interact and ultimately shape the evolutionary pathways taken by mimetic interactions, as well as the constraints inherent within these interactions.     

The evolution of mimicry under constraints

The resemblance between mimetic organisms and their models varies from near perfect to very crude. One possible explanation, which has received surprisingly little attention, is that evolution can improve mimicry only at some cost to the mimetic organism. In this article, an evolutionary game theory model of mimicry is presented that incorporates such constraints. The model generates novel and testable predictions. First, Batesian mimics that are very common and/or mimic very weakly defended models should evolve either inaccurate mimicry (by stabilizing selection) or mimetic polymorphism. Second, Batesian mimics that are very common and/or mimic very weakly defended models are more likely to evolve mimetic polymorphism if they encounter predators at high rates and/or are bad at evading predator attacks. The model also examines how cognitive constraints acting on signal receivers may help determine evolutionarily stable levels of mimicry. Surprisingly, improved discrimination abilities among signal receivers may sometimes select for less accurate mimicry.     

Male cleaner wrasses adjust punishment of female partners according to the stakes

Punishment is an important deterrent against cheating in cooperative interactions. In humans, the severity of cheating affects the strength of punishment which, in turn, affects the punished individual's future behaviour. Here, we show such flexible adjustments for the first time in a non-human species, the cleaner wrasse (Labroides dimidiatus), where males are known to punish female partners. We exposed pairs of cleaners to a model client offering two types of food, preferred 'prawn' items and less-preferred 'flake' items. Analogous to interactions with real clients, eating a preferred prawn item ('cheating') led to model client removal. We varied the extent to which female cheating caused pay-off reduction to the male and measured the corresponding severity of male punishment. Males punished females more severely when females cheated during interactions with high value, rather than low value, model clients; and when females were similar in size to the male. This pattern may arise because, in this protogynous hermaphrodite, cheating by similar-sized females may reduce size differences to the extent that females change sex and become reproductive competitors. In response to more severe punishment from males, females behaved more cooperatively. Our results show that punishment can be adjusted to circumstances and that such subtleties can have an important bearing on the outcome of cooperative interactions.