Protective Mimicry Research Articles

Cleaner fish coloration does not always reduce predation risk: testing the effect of protective mimicry in the false cleanerfish, Aspidontus taeniatus

Abstract Cleaning symbiosis of the bluestreak cleaner wrasse, Labroides dimidiatus (Labridae), is a well-known example of mutualism in coral reefs. The cleaner wrasse is characterized by its bluish body colour with black stripes, and the false cleanerfish, Aspidontus taeniatus (Blenniidae), mimics those characteristics precisely. Cleaner fish mimicry is believed to evolve as an aggressive mimicry to bite the fins of deceived fishes; however, protective mimicry to reduce predation risk has not been examined sufficiently. Here, we tested the effect of protective mimicry through field observations and aquarium experiments. Field observations revealed that false cleanerfish were occasionally attacked by piscivorous lizardfishes (Synodontidae). In the aquarium experiments, ambushing predators, the honeycomb grouper, Epinephelus merra (Serranidae), which did not show predatory behaviour to false cleanerfish in the field, attacked the cleaner wrasse (model), the false cleanerfish (mimic), and the lance blenny, Aspidontus dussumieri (non-mimic). When a shelter was provided in the tank, the false cleanerfish and the lance blenny immediately hid inside the shelter for a considerable duration to escape from the predator. These results suggest that cleaner fish coloration does not always decrease predation risks, and our conclusions support the possibility that this mimicry evolved primarily as aggressive mimicry.

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

The online version contains supplementary material available at 10.1007/s10164-022-00769-8.

A case for mutualistic deceptive mimicry

Abstract It has long been understood that species that are profitable for predators to attack can gain protection if they resemble unprofitable species (Batesian mimicry), and that unprofitable species may face selection to evolve a common warning signal (Müllerian mimicry). Here we suggest that there may be widespread selection for another form of protective mimicry, so far unrecognized, that can arise even among profitable prey. Specifically, when predators adopt species-specific attack strategies, then co-occurring prey species that are caught in different ways may be selected to resemble one another. This is because the mimicry may increase the chance that the predator deploys an inappropriate attack strategy, thereby increasing the probability the prey will escape. We refer to this phenomenon as “mutualistic deceptive mimicry”, since the mimicry misleads the predator yet potentially benefits all co-mimics. We show that this hypothesis is quantitatively plausible. We then provide an empirical ‘proof of concept’ demonstrating that predators can learn to attack distinct prey types in specific ways and that this behaviour readily generates selection for mimicry. Finally, we discuss how this unrecognized form of mimicry fits into an earlier classification of protective mimicry and suggest a number of potential examples in the natural world.

Aggressive mimicry in a coral reef fish: The prey's view.

Since all forms of mimicry are based on perceptual deception, the sensory ecology of the intended receiver is of paramount importance to test the necessary precondition for mimicry to occur, that is, model‐mimic misidentification, and to gain insight in the origin and evolutionary trajectory of the signals. Here we test the potential for aggressive mimicry by a group of coral reef fishes, the color polymorphic Hypoplectrus hamlets, from the point of view of their most common prey, small epibenthic gobies and mysid shrimp. We build visual models based on the visual pigments and spatial resolution of the prey, the underwater light spectrum and color reflectances of putative models and their hamlet mimics. Our results are consistent with one mimic‐model relationship between the butter hamlet H. unicolor and its model the butterflyfish Chaetodon capistratus but do not support a second proposed mimic‐model pair between the black hamlet H. nigricans and the dusky damselfish Stegastes adustus. We discuss our results in the context of color morphs divergence in the Hypoplectrus species radiation and suggest that aggressive mimicry in H. unicolor might have originated in the context of protective (Batesian) mimicry by the hamlet from its fish predators rather than aggressive mimicry driven by its prey.

The Evolutionary Importance of Cues in Protective Mimicry

The Evolutionary Importance of Cues in Protective Mimicry

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

AbstractThe 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.

Walking like an ant: a quantitative and experimental approach to understanding locomotor mimicry in the jumping spider Myrmarachne formicaria.

Protective mimicry, in which a palatable species avoids predation by being mistaken for an unpalatable model, is a remarkable example of adaptive evolution. These complex interactions between mimics, models and predators can explain similarities between organisms beyond the often-mechanistic constraints typically invoked in studies of convergent evolution. However, quantitative studies of protective mimicry typically focus on static traits (e.g. colour and shape) rather than on dynamic traits like locomotion. Here, we use high-speed cameras and behavioural experiments to investigate the role of locomotor behaviour in mimicry by the ant-mimicking jumping spider Myrmarachne formicaria, comparing its movement to that of ants and non-mimicking spiders. Contrary to previous suggestions, we find mimics walk using all eight legs, raising their forelegs like ant antennae only when stationary. Mimics exhibited winding trajectories (typical wavelength = 5–10 body lengths), which resemble the winding patterns of ants specifically engaged in pheromone-trail following, although mimics walked on chemically inert surfaces. Mimics also make characteristically short (approx. 100 ms) pauses. Our analysis suggests that this makes mimics appear ant-like to observers with slow visual systems. Finally, behavioural experiments with predatory spiders yield results consistent with the protective mimicry hypothesis. These findings highlight the importance of dynamic behaviours and observer perception in mimicry.

More than meets the eye: change in pupil shape by a mock viper

More than meets the eye: change in pupil shape by a mock viper

Breaking Down What Matters: Welcome to COMpostINGS

Breaking Down What MattersWelcome to compostings Michaela Castellanos (bio) This issue of Resilience features the first installation of a new series called compostings. Two at a time, the essays in this series will explore concepts that influence how we think about our myriad relationships with our animate and inanimate nonhuman others. They will do so, for example, by reflecting on unwieldy and polysemous concepts in a way that appreciates their complexity. Will Abberley's essay on biological mimicry starts off the series in this spirit. Based on the assumption that insects and plants intentionally disguise themselves to trick predators, the idea of protective mimicry at first seems to derive from an anthropocentric bias. Yet mimicry undermines the human/animal binary, Abberley argues, as it frames animals as interpretive agents rather than passive machines. Probing the entanglement of mimicry with intentionality, anthropomorphism, umwelt, and finally empathy, he shows that this concept challenged the growing discourse of scientific objectivity and rejection of anthropomorphism already in the nineteenth century. The compostings series also emphasizes transcultural flows in environmental thinking. Jonathan Beever's essay points out a historical connection between American conservationist Aldo Leopold and Estonian-born biologist Jakob von Uexküll. Beever identifies a pivotal shift in Leopold's developing thought about the moral value of the natural world. Arguing that Leopold's ethical attention turns from the biotic whole to living individuals, he links this change to the intellectual influence of Uexküll, which he then shows in Leopold's private and public writing. [End Page 60] Literature is central to both Beever and Abberley's explorations. When approaching the individual/whole dichotomy as an ethical problem, Beever turns to the iconic "green fire" passage in A Sand County Almanac (1949); Abberley traces the anxieties about mimicry in Tomas Belt's The Naturalist in Nicaragua (1874). On a subordinated level, both essays reflect on the Uexküllian notion of umwelt from a particular disciplinary perspective—ethics and literary studies. The essays thus come together in an unexpected way, which creates a productive synergy that I hope will also emerge from future compostings. In "An Attempt at a 'Compositionist Manifesto,'" Bruno Latour praises the term compositionist for the variety of connotations it imports, and among those is the "pungent but ecologically correct smell of 'compost,' itself due to the active 'de-composition' of many invisible agents."1 If compostings decompose concepts in order to reassemble them in different form, the series responds to Latour's call to cultivate compositionism as a successor to nature and as an alternative to critique.2 In Latour's words, It is a really mundane question of having the right tools for right job. With a hammer (or a sledge hammer) in hand you can do a lot of things: break down walls, destroy idols, ridicule prejudices, but you cannot repair, take care, assemble, reassemble, stitch together.3 A heartfelt thank you to the first contributors for breaking down and reassembling what matters to them! Michaela Castellanos Michaela Castellanos is a PhD candidate in English at Mid-Sweden University in Sundsvall, Sweden. Her main areas of academic inquiry are animal studies and the environmental humanities. Her current research project is concerned with representations of cetaceans in contemporary American popular culture. She is the current webinar coordinator for the European Association for the Study of Literature, Culture, and the Environment (easlce) and the European editor of Resilience: A Journal of the Environmental Humanities. notes 1. Latour, "Attempt at a 'Compositionist Manifesto,'" 473–74. 2. Latour, "Attempt at a 'Compositionist Manifesto,'" 477. 3. Latour, "Attempt at a 'Compositionist Manifesto,'" 475. [End Page 61] references Belt, Thomas. The Naturalist in Nicaragua. London: John Murray, 1874. Google Scholar Latour, Bruno. "An Attempt at a 'Compositionist Manifesto.'" New Literary History 41 (2010): 471–90. Google Scholar Leopold, Aldo. A Sand County Almanac and Sketches Here and There. New York: Oxford University Press, 1949. [End Page 62] Google Scholar Copyright © 2017 University of Nebraska Press

Mimicry in Lolita

In his study of butterflies Vladimir Nabokov was fascinated by mimicry, the techniques of camouflage and defense that the prey uses to protect itself from the predator. Writing to a publisher on Nabokov’s behalf in 1952, his wife Vera confirmed his longstanding interest in this subject: “the question of mimicry is one that has passionately interested him all his life, and one of his pet projects has always been the compilation of a work that would comprise all the known examples of mimicry in the animal kingdom.” In Lolita (1955), Nabokov creates a world where the characters employ human variants of insect strategies. They adopt masks and mirrors, personae and pretense, imitation and illusion to disguise and deceive. Despite the elaborate strategies of protective mimicry, all the characters in Lolita , like insects, have brief lives that end abruptly. Humbert’s mother had been struck by a thunderbolt: “picnic, lightning.” His childhood love, Annabel Lee, had died of typhus in Corfu. His first wife, Valeria, had died in childbirth. All four principal characters are doomed and at the end of the novel they are all dead. Charlotte is hit by a car, Lolita (like Valeria) dies giving birth to a child. In a protracted and vengeful scenario, Humbert murders Quilty, is condemned to death and dies of a heart attack in prison. Uniting lepidoptery and art with consummate style and wit, Nabokov wrote the greatest novel by any writer trained in science.

Resembling a viper: implications of mimicry for conservation of the endangered smooth snake.

The phenomenon of Batesian mimicry, where a palatable animal gains protection against predation by resembling an unpalatable model, has been a core interest of evolutionary biologists for 150 years. An extensive range of studies has focused on revealing mechanistic aspects of mimicry (shared education and generalization of predators) and the evolutionary dynamics of mimicry systems (co-operation vs. conflict) and revealed that protective mimicry is widespread and is important for individual fitness. However, according to our knowledge, there are no case studies where mimicry theories have been applied to conservation of mimetic species. Theoretically, mimicry affects, for example, frequency dependency of predator avoidance learning and human induced mortality. We examined the case of the protected, endangered, nonvenomous smooth snake (Coronella austriaca) that mimics the nonprotected venomous adder (Vipera berus), both of which occur in the Åland archipelago, Finland. To quantify the added predation risk on smooth snakes caused by the rarity of vipers, we calculated risk estimates from experimental data. Resemblance of vipers enhances survival of smooth snakes against bird predation because many predators avoid touching venomous vipers. Mimetic resemblance is however disadvantageous against human predators, who kill venomous vipers and accidentally kill endangered, protected smooth snakes. We found that the effective population size of the adders in Åland is very low relative to its smooth snake mimic (28.93 and 41.35, respectively).Because Batesian mimicry is advantageous for the mimic only if model species exist in sufficiently high numbers, it is likely that the conservation program for smooth snakes will fail if adders continue to be destroyed. Understanding the population consequences of mimetic species may be crucial to the success of endangered species conservation. We suggest that when a Batesian mimic requires protection, conservation planners should not ignore the model species (or co-mimic in Mullerian mimicry rings) even if it is not itself endangered.

Evolutionary implications of deception in mimicry and masquerade

Abstract Aggressive mimicry occurs when an organism resembles some aspect of another organism (the model) in order to obtain prey through its deceptive resemblance. This may function either through the overt response of the receiver or through the lack of response of the receiver. Reviewing selected examples, I discuss some of the difficulties in ascribing a model for the mimic. I also discuss how a single animal can have multiple ploys in its armoury of deceptive signals, thus belonging within two or more categories of deceptive signalling. In addition to aggressive mimicry, these may include crypsis or camouflage, masquerade (mimicry of inanimate objects), and Batesian or protective mimicry. Each of these examples of deception has multiple evolutionary pathways, and some deceptive signals may be more costly to receivers than others, but no single organism is subject to a single selection pressure, leading to the reality that many evolutionary pathways contribute to the diversity we see around us. New technologies are opening new channels of investigation into deceptive signaling in many different sensory modalities, and this is reflected in the recent increase in studies investigating the structure and function of deceptive signals. In turn, these studies are beginning to expose the fascinating complexity of deceptive signaling systems, allowing us to discover the myriad, non-mutually exclusive, solutions that can be selected for to obtain prey.

Geographical variation in the benefits obtained by a coral reef fish mimic

Mimicry systems are frequently categorized by the type of benefit gained by the mimic's resemblance to its model: protection from threat, including predation (protective mimicry), and increased access to resources, including prey items (aggressive mimicry). These category types may not be mutually exclusive, and some mimics may gain more than one type of benefit. Here we examined a contentious classic textbook example of mimicry between the cleaner wrasse Labroides dimidiatus and its mimic, the sabre-toothed blenny Aspidontus taeniatus. We found that the benefit obtained by the sabre-toothed blenny varied between four geographical locations. At the Great Barrier Reef, in Indonesia and in the Red Sea, it rarely attacked reef fish victims, but instead relied on other food sources such as substrate items, damselfish eggs and tubeworms. Here, the main function of the mimicry system could be to protect the sabre-toothed blenny from predation (protective mimicry) and was consistent with a previous study in Japan. However, in French Polynesia, the sabre-toothed blenny aggressively attacked reef fish frequently, and potential victims were more likely to pose to solicit a cleaning interaction. Diet analysis from individuals in French Polynesia indicated material was gleaned from the surface of fish, including large pieces of fin, implying an increase in the benefits obtained from attacking reef fish (aggressive mimicry). This study provides a potential second example of a mimicry system in which multiple types of benefits are gained by a mimic, and importantly, that the benefits obtained by the mimic vary between different environmental conditions and/or geographical locations. This may have important implications for the maintenance and evolution of mimicry systems and may reflect different stages of an arms race with potential victims.

Cuckoos Combat Socially Transmitted Defenses of Reed Warbler Hosts with a Plumage Polymorphism

In predator-prey and host-parasite interactions, an individual's ability to combat an opponent often improves with experience--for example, by learning to identify enemy signals. Although learning occurs through individual experience, individuals can also assess threats from social information. Such recognition could promote the evolution of polymorphisms if socially transmitted defenses depend on enemy morph frequency. This would allow rare variants to evade detection. Female brood parasitic common cuckoos, Cuculus canorus, are either gray or rufous. The gray morph is a Batesian mimic whose hawk-like appearance deters host attack. Hosts reject this disguise through social learning, increasing their own defenses when they witness neighbors mobbing a cuckoo. Our experiments reveal that social learning is specific to the cuckoo morph that neighbors mob. Therefore, while neighbors alert hosts to local cuckoo activity, frequency-dependent social information selects for a cuckoo plumage polymorphism to thwart host detection. Our results suggest that selection for mimicry and polymorphisms comes not only from personal experience but also from social learning.

Mixed-species schooling behavior and protective mimicry involving coral reef fish from the genus Haemulon (Haemulidae)

The present study analyzed heterotypic schooling behavior and protective mimicry relationships involving species of the genus Haemulon and other coral reef fishes on coastal reefs at Tamandaré, Pernambuco State, Northeastern Brazil. The work was performed during 35 hours of direct observation using the "focal animal" method. The observed events involved 14 species of reef fish in eight different families. The phenomenon of mixed schooling appeared to be related to the large number of individuals of the genus Haemulon present in reef environments and to the tendency of individuals with limited populations to try to aggregate in schools (e.g. genus Scarus).

"Protective Mimicry": Forster's Literary Imitation of 'Divide and Rule' in A Passage to India

Critical response to E. M. Forster's A Passage to India remains diverse. While some commend Forster's depiction of the India, others express their misgivings at his portrayal of Indians attributing his delineation of the Indians, their behaviors, their religions and customs, even the geographical landscape to be in the Orientalist tradition. While looking at the historical bases of A Passage to India, this paper establishes that being conscious of the British administration's policy of 'divide and rule,' Forster undertakes a similar exercise of widening the gulf between the Hindus and Muslims. Forster's 'knowledge' of the political conditions in India and Europe, the differences between the two communities and his imperial anxieties pertaining to the future of the British Empire shapes his representation of Hindus and Muslims as two distinct 'types,' as a form of literary mimicry of the British policy of 'divide and rule.' This paper also argues that A Passage to India's importance as a seminal colonial text in India has helped reinforce this difference in the Indian consciousness and continues to foment communal riots in the country even ninety years after its publication

The role of avoidance learning in an aggressive mimicry system

Batesian mimicry systems are driven by predators that learn to associate a distinct signal with an unpalatable species and then avoid similar signals on future occasions, including those emitted by palatable mimics. Whereas many studies have investigated learning and predator memory in protective mimicry, few studies have considered learning in other mimicry systems. Aggressive mimics are defined as the resemblance of a predatory or parasitic species to another nonthreatening or even attractive species in order to approach and attack prey or to gain other benefits such as pollination or transportation. If signal receivers learn to avoid aggressive mimics and their models or learn to distinguish mimics from their models, then the success of mimics should decline. On coral reefs, juvenile bluestreak cleaner fish (Labroides dimidiatus) are aggressively mimicked by the bluestriped fangblenny (Plagiotremus rhinorhynchos). Instead of removing parasites from larger host fish, fangblennies attack reef fish and remove scales and dermal tissue. In this study, the signal receiver (a damselfish) spatially avoided cleaner fish and their associated fangblenny mimics after aggressive interactions; however, avoidance was not exhibited for longer than 24 h. Damselfish did not appear to discriminate between cleaner fish and mimic fangblenny, however, did discriminate between cleaner fish and nonmimic fangblenny. Avoidance learning was more pronounced when the fangblenny was less similar to the cleaner fish in terms of color. Finally, damselfish learnt to preempt attacks within 1 h of contact with fangblennies. This study provides important insights into the role of both spatial and preemptive avoidance learning in aggressive mimicry

COMPETITIVE MIMICRY: SYNTHESIS OF A NEGLECTED CLASS OF MIMETIC RELATIONSHIPS

Protective mimicry has been studied extensively for over a century. Mimicry in a competitive context, however, has remained largely neglected. It has been overlooked in mimicry classification schemes, and few systems have been rigorously studied. We define "competitive mimicry" as mimicry that enables access to a defended resource or aids in defense of a resource. We explain how competitive mimicry fits with existing mimicry classification schemes and outline criteria for identifying competitive mimicry systems. For each form of competitive mimicry, we describe the effects of the mimic on the model and receiver, predict the evolutionary dynamics of the system, and present examples. We then identify key directions for the study of competitive 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 association of the goatfish mulloidichthys martinicus with the grunt haemulon chrysargyreum: an example of protective mimicry

A presumed example of protective mimicry between the yellow goatfish, Mulloidichthys martinicus (Mullidae) and the smallmouth grunt, Haemulon chrysargyreum (Haemulidae) is described from Fernando de Noronha Archipelago, NE Brazil. The goatfish and the grunt share a similar overall shape and colour pattern. We found that these two species regularly form mixed schools around reefs. Additionally, when chased small groups of yellow goatfish join schools of smallmouth grunts and behave like them. The colour and shape resemblances between the two species enable their mixed schooling, and enhance the protection against visually oriented predators for both of them. Thus, we suggest that the protective association herein reported for the goatfish and the grunt may be considered as a “social mimicry”, since neither species is venomous, poisonous or strongly armed. Furthermore, we suggest that additional instances of social mimicry may involve the yellow goatfish and other striped Haemulon species.