Aggressive Mimicry Research Articles

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.

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.

Convergent evolution of eye ultrastructure and divergent evolution of vision‐mediated predatory behaviour in jumping spiders

All jumping spiders have unique, complex eyes with exceptional spatial acuity and some of the most elaborate vision-guided predatory strategies ever documented for any animal of their size. However, it is only recently that phylogenetic techniques have been used to reconstruct the relationships and key evolutionary events within the Salticidae. Here, we used data for 35 species and six genes (4.8 kb) for reconstructing the phylogenetic relationships between Spartaeinae, Lyssomaninae and Salticoida. We document a remarkable case of morphological convergence of eye ultrastructure in two clades with divergent predatory behaviour. We, furthermore, find evidence for a stepwise, gradual evolution of a complex predatory strategy. Divergent predatory behaviour ranges from cursorial hunting to building prey-catching webs and araneophagy with web invasion and aggressive mimicry. Web invasion and aggressive mimicry evolved once from an ancestral spartaeine that was already araneophagic and had no difficulty entering webs due to glue immunity. Web invasion and aggressive mimicry was lost once, in Paracyrba, which has replaced one highly specialized predation strategy with another (hunting mosquitoes). In contrast to the evolution of divergent behaviour, eyes with similarly high spatial acuity and ultrastructural design evolved convergently in the Salticoida and in Portia.

Colour pattern as a single trait driving speciation inHypoplectruscoral reef fishes?

Theory shows that speciation in the presence of gene flow occurs only under narrow conditions. One of the most favourable scenarios for speciation with gene flow is established when a single trait is both under disruptive natural selection and used to cue assortative mating. Here, we demonstrate the potential for a single trait, colour pattern, to drive incipient speciation in the genus Hypoplectrus (Serranidae), coral reef fishes known for their striking colour polymorphism. We provide data demonstrating that sympatric Hypoplectrus colour morphs mate assortatively and are genetically distinct. Furthermore, we identify ecological conditions conducive to disruptive selection on colour pattern by presenting behavioural evidence of aggressive mimicry, whereby predatory Hypoplectrus colour morphs mimic the colour patterns of non-predatory reef fish species to increase their success approaching and attacking prey. We propose that colour-based assortative mating, combined with disruptive selection on colour pattern, is driving speciation in Hypoplectrus coral reef fishes.

Phoretic nest parasites use sexual deception to obtain transport to their host's nest.

Cooperative behaviors are common among social insects such as bees, wasps, ants, and termites, but they have not been reported from insect species that use aggressive mimicry to manipulate and exploit prey or hosts. Here we show that larval aggregations of the blister beetle Meloe franciscanus, which parasitize nests of the solitary bee Habropoda pallida, cooperate to exploit the sexual communication system of their hosts by producing a chemical cue that mimics the sex pheromone of the female bee. Male bees are lured to larval aggregations, and upon contact (pseudocopulation) the beetle larvae attach to the male bees. The larvae transfer to female bees during mating and subsequently are transported to the nests of their hosts. To mimic the chemical and visual signals of female bees effectively, the parasite larvae must cooperate, emphasizing the adaptive value of cooperation between larvae. The aggressive chemical mimicry by the beetle larvae and their subsequent transport to their hosts' nests by the hosts themselves provide an efficient solution to the problem of locating a critical but scarce resource in a harsh environment.

Mimicry in plant-parasitic fungi

Mimicry is the close resemblance of one living organism (the mimic) to another (the model), leading to misidentification by a third organism (the operator). Similar to other organism groups, certain species of plant-parasitic fungi are known to engage in mimetic relationships, thereby increasing their fitness. In some cases, fungal infection can lead to the formation of flower mimics (pseudo flowers) that attract insect pollinators via visual and/or olfactory cues; these insects then either transmit fungal gametes to accomplish outcrossing (e.g. in some heterothallic rust fungi belonging to the genera Puccinia and Uromyces) or vector infectious spores to healthy plants, thereby spreading disease (e.g. in the anther smut fungus Microbotryum violaceum and the mummy berry pathogen Monilinia vaccinii-corymbosi). In what is termed aggressive mimicry, some specialized plant-parasitic fungi are able to mimic host structures or host molecules to gain access to resources. An example is M. vaccinii-corymbosi, whose conidia and germ tubes, respectively, mimic host pollen grains and pollen tubes anatomically and physiologically, allowing the pathogen to gain entry into the host's ovary via stigma and style. We review these and other examples of mimicry by plant-parasitic fungi and some of the mechanisms, signals, and evolutionary implications.

Interactions between fangblennies (Plagiotremus rhinorhynchus) and their potential victims: fooling the model rather than the client?

Lepidophagous (scale-eating) blue-striped fangblennies (Plagiotremus rhinorhynchus Bleeker 1852) are often found sympatrically with the bluestreak cleaner wrasse (Labroides dimidiatus Valenciennes 1839). They have some resemblance to the juvenile L. dimidiatus and have previously been reported as aggressive cleaner wrasse mimics. We observed 14 P. rhinorhynchus on a small area in the barrier reef near Hoga Island, Indonesia to assess the effects of client size on the behaviour and attack success of fangblennies: our results suggest that fangblennies are selective with regard to victim size; fish avoided by the fangblennies are significantly larger than those not avoided and attack success is significantly higher at intermediate victim size classes. The behaviour of the victims also has a significant direct effect on the foraging success of the fangblennies; where the potential victim posed, 63.6% were ignored by the fangblenny and only 7.4% of attacks were successful on posing fish as opposed to a surprise attack success rate of 71.6%. Overall, victims which exhibited the pose behaviour were significantly smaller in size. It appears likely that the predatory strategy of these fangblennies varies with victim size and that mimicry plays a minor role in attracting potential victims. We suggest that in common with other mimetic fish the resemblance of fangblennies to juvenile bluestreak cleaner wrasse allows them to actively hunt in areas where adult cleaners are common thus, indirectly improving their feeding opportunities.

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.

Genetic and Ecological Characterisation of Colour Dimorphism in a Coral Reef Fish

Many recognised species of coral reef fishes exhibit two or more colour variants, but it is unknown whether these represent genetically identical phenotypes, genetic polymorphisms or closely related species. We tested between these alternatives for two colour morphs of the coral reef fish, Pseudochromis fuscus, from Lizard Island (Great Barrier Reef). A molecular analysis using mtDNA did not detect any genetic differentiation between co-occurring ‘yellow’ and ‘brown’ colour morphs. A previous study proposed that these two colour morphs are aggressive mimics of yellow and brown damselfishes. Here, a manipulative field experiment was used to evaluate whether the colour dimorphism in P. fuscus is a phenotypic response to the presence of two different model species. Colonies of either yellow or brown damselfish species were established on different patch reefs, and each of the two different P. fuscus morphs was then placed on the different reefs. Contrary to expectations, all yellow individuals that stayed on the reefs changed to brown, regardless of the model species. No brown individuals changed to the yellow colouration. However, P. fuscus were more likely to emigrate from, or suffer higher mortality on, patch reefs where they were not matched with similarly coloured models. Clearly, yellow and brown P. fuscus are members of a single species with sufficient phenotypic plasticity to switch from yellow to brown colouration.

Wolf in a sheep's clothes: juvenile coney (Cephalopholis fulva) as an aggressive mimic of the brown chromis (Chromis multilineata)

We found yellowish juvenile coneys (Cephalopholis fulva) at Fernando de Noronha Archipelago, off Northeast Brazil, joining schools of similarly sized and coloured brown chromis (Chromis multilineata) when these latter closely approach the rocky reefs. Mingled within the mid-water hovering group of the plankton-feeding chromis, the piscivorous coney is able to approach unaware prey - an instance of aggressive mimicry. Three out of four coney individuals hunting under such disguise were successful in their attempts to prey on the otherwise wary rock-dwelling blenny (Malacoctenus species). This is the first instance of an epinepheline grouper mimicking a schooling and plankton-eating damselfish model in the West Atlantic.

Chapter One: Aggressive Mimicry: The Rhetoric of Wise Use and the Environmental Movement

Chapter One: Aggressive Mimicry: The Rhetoric of Wise Use and the Environmental Movement

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.

Specific color sensitivities of prey and predator explain camouflage in different visual systems

In situations of aggressive mimicry, predators adapt their color to that of the substrate on which they sit for hunting, a behavior that is presumed to hide them from prey as well as from their own predators. Females of few crab-spider species encounter such situations when lying on flowers to ambush pollinators. To evaluate the efficiency of spider camouflage on flowers, we measured by spectroradiometry adult female Thomisus onustus and marguerite daisies, Leucanthemum vulgare. We compared chromatic contrast (color used for short-range detection) of each pair of spider and flower to detection thresholds computed in the visual systems of both Hymenopteran prey and passerine bird predator. We also computed achromatic contrast (brightness) used for long-range detection. In both visual systems, each individual spider was efficiently matching the precise color of the flower center on which it was hunting. Being significantly darker than flowers, crab-spiders could in theory be detected at long range by either predator or prey using achromatic contrast. However, long-range detection is unlikely, owing to small spider size. Spiders also generated significant chromatic and achromatic contrasts to both Hymenoptera and bird when moving on flower periphery. Our study is the first to identify which photoreceptors of both prey and predator are involved in camouflage. The analysis suggests more research on bird predation and vision to determine to which extent bird predators effectively constrain spider crypsis.

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.

Ecological mechanisms for coexistence of colour polymorphism in a coral-reef fish: an experimental evaluation.

The evolution of different colour morphs and how they are maintained in animal populations is poorly understood. We investigated the mechanisms maintaining yellow and brown morphs of a coral-reef fish, Pseudochromis fuscus, at Lizard Island, on the Great Barrier Reef. Histological examination of the gonads revealed that colour morphs were not sex-limited, therefore sexual selection does not appear to promote dichromatism in this species. The field distributions of the two colour morphs were spatially segregated, limiting the opportunity for negative frequency-dependent selection to operate. Our results support another ecological mechanism of coexistence. The yellow morph occurred in deeper areas, usually close to the reef edge, where there was a proportionally high cover of live branching corals. In contrast, the brown morph occurred in shallower areas, more distant from the reef edge, that were proportionally low in live branching corals. Within these habitats, each colour morph of P. fuscus displayed a close association with similar coloured damselfishes from the genus Pomacentrus. The yellow morph was associated with predominantly yellow damselfishes (P. moluccensis and P. amboinensis) and the brown morph with darker coloured species (P. adelus and P. chrysurus). Multiple-choice experiments in the laboratory revealed that: (1) each colour morph of P. fuscus preferentially selected habitat patches occupied by damselfishes with the same colouration; and (2) differences in microhabitat use between the two colour morphs of P. fuscus were due to the presence of different coloured damselfishes in these microhabitats. P. fuscus is a predator of newly recruited damselfishes and the striking resemblance between each morph of P. fuscus and the damselfish with which it was associated, suggests that aggressive mimicry may promote coexistence of P. fuscus colour morphs.

True and false threatening visual cues in some Mediterranean fish

Mediterranean fish of the Trachinidae and Uranoscopidae families are characterized by a poison apparatus on the 1st dorsal fin. These fish hide by burying themselves in the sand using cryptic mimicry. Nevertheless, if they are discovered before they have completely buried themselves, or perceive a potential source of danger when already covered, they will raise their 1st dorsal fin which has a bright black spot on the inter-radial membrane. We have shown that this black vexillum acts as a threatening visual cue and that the movements accompanying black mark display can be defined as aggressive mimicry. We therefore thought it interesting to investigate the black mark display in some species of Soleidae, a behaviour never before reported in the literature. In these fish, the black marks are situated on the right pectoral fin which, as a result of the distortion and re-arrangement of some anatomical parts during development, shifts to a dorsal position in adults. Soles also bury themselves in the sand, and they too display their marked fins on the approach of a possible predator, just like fish belonging to the above dangerous families.

The spider and fly revisited: ploy-counterploy behavior in a unique predator-prey system

Earlier studies have shown that the sarcophagid fly Arachnidomyia lindae is the principal egg-sac predator of the colonial orb-weaving spider Metepeira incrassata, and that risk of egg-sac loss increases with group size. Observations of specialized behaviors for attack (flies) and defense (spiders) suggest that this predator–prey relationship may incorporate elements of ploy and counterploy behavior. Here we explore this relationship in detail and test hypotheses regarding efficacy of attack and defense behaviors. Egg-sac guarding by the spider includes defensive behaviors specific to this fly predator, which were observed during experimental "attacks" with tethered A. lindae, but not with similar presentations of non-predatory Musca domestica. Experimental studies also show that Metepeira incrassata recognizes this predatory fly by airborne cues (i.e., the signature frequency of wing-beats), and can distinguish between this predator and other flies (potential prey) on the basis of wing-beat frequency differences. Removal of female spiders results in a significantly higher probability of unguarded egg-sacs being parasitized, demonstrating the adaptive value of spider defensive behaviors. We also present evidence that A. lindae utilizes a behavioral ploy for circumventing spider guarding behavior (aggressive mimicry – producing vibrations of captured prey in the web), and that Metepeira incrassata, in turn, exhibits a counter-ploy behavior (signal thread cutting) to eliminate this potentially distracting vibratory information. While previous studies have shown that this colonial web-building spider uses a number of general attack-abatement mechanisms against a diversity of predators and parasitoids, results of this study suggest that selection pressures from a highly specialized predator may also result in evolution of predator-specific prey responses.

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.

Mimicry complex in two central European zodariid spiders (Araneae: Zodariidae): how Zodarion deceives ants

Ant-eating spiders, Zodarion germanicum and Z. rubidum, were found to resemble ants structurally (size, colour, setosity) and behaviourally (ant-like movement, antennal illusion). Zodarion germanicum mimics large dark ants, such as Formica cinerea, whereas Z. rubidum resembles red ants, e.g. Myrmica sabuleti. Thus, these spiders are generalized Batesian mimics. The two spiders use aggressive mimicry during prey capture. When a spider carries a captured ant it will try to pass by approaching ants using special deceiving behaviour, which is based on imitation of ants’ nestmate recognition. The spider first taps the antennae of the curious ant with its front legs (transmitting a tactile cue), then exposes its prey (the ant corpse) which the ant antennates (thus the corpse transmits an olfactory cue). The distal part of the front legs of Zodarion are almost without macrosetae similar to the antennae of ants. Additionally, all the other legs are covered with flattened incised setae, which imitate the dense setosity of ants’ limbs. These remarkable microstructural imitations are believed to improve imitation of tactile signals by spiders. Moreover, by tapping, zodariids can presumably recognize the approaching intruder and decide whether to undertake the risk of deception or to run away. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75, 517‐532. ADDITIONAL KEYWORDS: aggressive mimicry ‐ ants ‐ Araneae ‐ Batesian mimicry ‐ behaviour ‐ setosity ‐ tactile cue ‐ Zodarion.

Trial‐and‐error derivation of aggressive‐mimicry signals by Brettus and Cyrba, spartaeine jumping spiders (Araneae: Salticidae) from Israel, Kenya, and Sri Lanka

Brettus adonis, Brettus albolimbatus, Cyrba algerina, Cyrba ocellata, and Cyrba simoni are spartaeine jumping spiders (Salticidae) that invade other spiders’ webs, make vibratory signals that deceive the resident spider (aggressive mimicry), then attack and eat the spider. The signal‐generation behaviour of each of these five species is investigated in the laboratory. Each species is characterised by flexible predatory behaviour, including use of a trial‐and‐error (generate‐and‐test) algorithm to derive appropriate aggressive‐mimicry signals: first broadcast an array of different signals, then choose particular signals as a consequence of feedback from the prey spider. However, in laboratory experiments, B. adonis and B. albolimbatus relied on trial‐and‐error significantly more often than did C. algerina, C. ocellata, and C. simoni. Maternal effects and variation in experience were minimised because all individuals tested were laboratory‐reared to the second and third generation under standardised conditions. Selection pressures that may have been responsible for evolution of different levels of flexibility are considered.