RSS Survival on the reef part 1: Masquerading under false colours

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    8 May 2007
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    Look at this amazing pair of Meiacanthus grammistes. Eh hmm…wait a minute. That’s not quite right. Look closer. Cardinal fish? Bingo. This is a pair of Cheilodipterus nigrotaeniatus and they are excellent mimics of their venomous fang blenny models. Mimicry is an age old evolutionary strategy for survival, and comes in various forms. Mimicry encompasses protective resemblance, in which animals take on the form of inanimate objects to blend in and protect themselves; as well as mimesis proper, where mimics imitate their models for protection and various other reasons. In this article we explore some well known examples of mimicry and how this relationship affects their life on the reef. 

    [​IMG]Papilio memnon is a world famous butterfly species that exhibit batesian mimicry. The females are faithful copies of their corresponding models and come in more than a dozen forms across its range.

    When the subject of mimicry is raised, the first thing that comes to mind would probably be insects. Insects hold some of the world’s most classic examples of mimicry, and many have been extensively studied. There are many models for mimicry, but two well known examples include batesian and müllerian mimicry. In batesian mimicry, a vulnerable harmless species copies a poisonous model in its range to seek protection from predators.

    Again, this is a very common phenomenon in the world of insects, especially butterflies. In the example above, Papilio memnon is a harmless swallowtail butterfly species where only the female sex displays batesian mimicry. The females come in more than a dozen forms across their range, and each form (lower row) is a faithful copy of their poisonous model (upper row). The mimic model relationship works only in species whose range overlaps, and predators who identify with the unpalatable models will learn to avoid the mimic. This allows the harmless butterfly to gain protection by masquerading under false colours.

    In müllerian mimicry, two or more equally poisonous or distasteful species share very similar or nearly identical pattern and appearances. This raises the question that if both, or all are equally harmful, what is the need of copying each other? If two müllerian mimics were confused with one another by a common predator, individuals in both would be more likely to survive. In a sense this skews towards mutualism where having numerous poisonous sisters would decrease the chances of being eaten.

    [​IMG]A harmless perfectly edible Soleichthys maculosus flounder mimics the highly toxic flatworm Pseudoceros scintillates. Photo by Ned DeLoach.

    In the world of reef fish, batesian mimicry is more commonly observed, and is prevalent in a few group of shallow water species. For mimesis to work, both model and mimic would have to occupy the same niche and range. In many cases, the model not only copies the appearance, but also the behaviour. In the previously mentioned butterfly example, poisonous species are usually tenacious of life and are confident in their aposematic coloration. They adopt an unhurried and leisure flight. The harmless mimics being coloured the same way are also forced to mimic the same behavioural flight pattern to fully execute their disguise. Likewise in reef fish, both physical and behavioural mimesis takes place. The flounder Soleichthys maculosus above for example, mimics a poisonous flatworm species below.

    [​IMG]The toxic Pseudoceros scintillatus is the model for the harmless flounder above. Photo by Jim Anderson.

    Not only does the flounder copy the appearance of the worm, it takes things to the next level by moving in the exact same fashion. This video shows just what we’re talking about. Unlike a typical flounder fashion, S. maculosus moves by gliding and undulating its peripheral fins in the same way the flatworm does. In an effort to replicate the behaviour of its model, the fish hardly swims, and crawls around the sand bed. Under normal circumstances this would make any fish extremely vulnerable to predation, but the flounder is so confident in its mimicry that it throws all caution to the wind.

    [​IMG]The harmless Paraluterus prionurus on the left swims with its toxic model Canthigaster valentini on the right. Photo from Flickr user Romblon.

    Another classic case of batesian mimicry involves the harmless Paraluterus prionurus filefish and its highly unpalatable model, the Canthigaster valentini pufferfish. The mimesis is so successful that even humans tend to mix up the two, and many images of C. valentini are invariably wrongly named. Only upon close scrutiny does one realise that the puffer fish lacks the retractable file on the head. The filefish has also larger dorsal and anal fins. To a potential predator on the reef, these details are too minute to notice, and the warning coloration adopted by the puffer and the one copied by the mimic will suffice in deterrence.

    [​IMG]Meiacanthus geminatus (A) is the model for two harmless fishes. Juveniles of Scolopsis margaritifera (B) and Cheilodipterus zonatus (C) take on the colours of their venomous model. Photo credits A – Roger Steene. B – John E. Randall. C – Gerald R. Allen.

    Perhaps the most classic example on the reef for batesian mimicry revolves around the genus Meiacanthus. Meiacanthus are not poisonous or toxic species, but they are venomous. All of them. Although peaceful and usually non confrontational, predators have learned to avoid Meiacanthus because of their venomous bite. The lower jaw of all Meiacanthus species are equipped with two upward pointing sabre like fangs, with an inbuilt venom sac. They can deliver a painful bite when provoked. As such, a multitude of species in an array of genera have learnt to copy the venomous Meiacanthus. While most seek mimicry only as a form of protection, some malicious species have gone the extra mile and have used this to their advantage.

    In the example above, Meiacanthus geminatus plays the model role for two harmless reef fishes. Scolopsis margaritefera (B) is a bream capable of growing to moderately large sizes. However in its vulnerable juvenile stage, it seeks protection from predators by disguising as M. geminatus. Just like the bream, the cardinal fish Cheilodipterus zonatus also rides the tailcoat of its venomous model.

    [​IMG]An assortment of Meiacanthus species and their respective copies. A1- Meiacanthus nigrolineatus. A2- Plagiotremus townsendi. A3- Ecsenius gravieri. B1- Meiacanthus smithi. B2- Plagiotremus phenax. B3- Scolopsis bilineatus. C1- Meiacanthus oualanensis. C2- Plagiotremus laudandus flavis. C3- Scoplopsis bilineatus. D1- Meiacanthus atridorsalis. D2- Plagiotremus laudandus. E- Meiacanthus grammistes and Scolopsis bilineatus. Photo credits in the same order, Sally Polack, Joe De Vroe, Richard Field, Mahiran, Unipara, Ahmed Abdul Rahman, Ryan Photography, Frank Bossen, Ryan Photography, Monsuke, Kojiro Gejima and Ned De Loach.

    This image collage above shows five species of Meiacanthus (A1-D1 and E), and well as their mimics. The second row (A2-D2) comprises of fishes in the genus Plagiotremus, who mimic their respective Meiacanthus models. Plagiotremus are species that display aggressive mimicry, which we will touch upon later. Row (A3-C3) are the harmless models that use mimicry only to avoid predation.

    Let us take a look an column A as an example. In the Red Sea, Meiacanthus nigrolineatus (A1) is the venomous Meiacanthus species. The predatory fang blenny Plagiotremus townsendi (A2) is a non poisonous predator of reef fish. Plagiotremus sneak up on unsuspecting reef fish where they bite a chunk of flesh, scale or fins as part of their diet. Because of their mimicry toward the venomous Meiacanthus, predators ignore and leave these Plagiotremus alone. This in turns allow the Plagiotremus blennies to get closer to their host and with the element of surprise, bite a chunk of flesh for consumption. Because of their mimesis, and their ability to use this to their advantage by sneaking up to prey, Plagiotremus display both batesian as well as aggressive mimicry. The comb tooth blenny Ecsenius gravieri (A3) is a harmless algae eating batesian mimic that benefits from the model-mimic colour copying.

    The entire horizontal row (A2-D2) depicts various Plagiotremus species and their corresponding Meiacanthus models above. B3, C3 and E depicts the harmless juvenile Scolopsis breams that like Ecsenius gravieri in A3, only copy the Meiacanthus for protection. However unlike the blenny, these breams lose the juvenile mimicry coloration as they grow older, as they are able to fend for themselves without the need for protection. Picture E shows both the model Meiacanthus grammistes and its mimic Scolopsis bilineatus swimming side by side. S. bilineatus comes in three juvenile forms, each mimicking the corresponding Meiacanthus species in their range.

    There are many other examples of aggressive mimicry involving various other Plagriotremus species. P. tapeinosoma for example, mimics Trachinops taeniatus (Hulafish) in New South Wales. Likewise, the harmless mimics copying their poisonous Meiacanthus models are plenty, and not only restricted to Ecsenius and Scolopsis. Petroscirtes breviceps and Amblygobius linki for example, mimic Meiacanthus grammistes and Meiacanthus anema respectively.

    [​IMG]A classic example of aggressive mimicry, with the model Labroides dimidiatus and the model Aspidontus taeniatus. Photo credits in clockwise fashion from top left – Okinawa Zukan, Fishwise Professional, Mark Rosenstein and Free Water Jp.

    Continuing on the topic of aggressive mimicry, none is more classic than the cleaner wrasse and its impostor. The cleaner wrasse Labroides dimidiatus is a welcomed sight in reefs, and enjoys the protection from various fearsome predators. Fishes such as groupers and other large fish eating species have learned the value and services provided by the cleaner wrasse, and do not eat them. The cleaner wrasse swims in an up down undulating fashion to display themselves, and customers in need of servicing swim up to these stations. The wrasse picks off parasites as well as dead or dying tissue on the body, and even inside the gaping jaws of normally fearsome predators. In turn for their service, they enjoy protection on the reefs.

    The false cleaner wrasse, Aspidontus taeniatus, is an excellent mimic of the former. Unlike the cleaner wrasse, this fish is not interested in cleaning anything and like Plagiotremus, Aspidontus eats the flesh and scales of other fish. By imitating the cleaner wrasse’s patterns down to the undulating swimming fashion, Aspidontus taeniatus is able to swim right up to unsuspecting fish, taking a bite off their host. Their mimicry is so precise that even certain regional coloration of Labroides dimidiatus are copied to the fullest. In Fiji for example, the cleaner wrasse sports a yellow patch on the distal portion of its black stripe, and Aspidontus living in this geographical region copies the yellow coloration as well.

    [​IMG]Centropyge models and their respective Acanthurid mimics. A- Centropyge flavissima. A- Acanthurus pyroferus. B- Centropyge vroliki. B1- Acanthurus pyroferus. C and C1- Centropyge eibli and Acanthurus pyroferus. Photos credits in the same above sequence, Nob@Feel The Sea, In-depth images Kwajalein, Zukan, In-depth images Kwajalein, Takeshi Omura and Ray.

    Another curious example of batesian mimicry revolves around Acanthurus pyroferus, and its ability to mimic at least four species of Centropyge. The juveniles of A. pyroferus is remarkable in being the only surgeonfish to display such striking mimesis. Depending on its range and the corresponding dwarf angelfish found there, the juveniles of A. pyroferus are rather good mimics of their models. It is curious, seeing as Centropyge species are neither venomous nor poisonous.

    A study done on this mimesis initially suggests that Centropyge, like Pomacanthus and Holacanthus, may provide part time cleaning services as juveniles. This would offer the angels some sort of protection against predation. However gut analysis failed to provide any evidence to support this theory. Randall suggested that the juvenile surgeonfish mimics the dwarf angels not because of they are unpalatability (they are edible), but rather for their cunning and sly nature. Centropyge are very weary, cunning and quick to retreat in the catacombs of the reefs, and are not only extremely difficult to chase after, they are also very difficult to catch. As such, many predators like groupers and snappers learn to avoid expending energy chasing after Centropyge and go for easier prey.

    Juveniles of A. pyroferus learn to mimic the pattern and coloration of certain Centropyge, and are often seen swimming beside or near them. In the photos C and C1 above, A. pyroferus is seen swimming alongside C. eibli. Because predators are often too lazy to chase after Centropyge and choose to go after slower species, the surgeonfish gains some form of protection, and is allowed to graze slowly on algae growing on the reef front.

    Mimicry is a vital and clever adaption for survival, and these clever reef fish have proven themselves worthy to fight another day.
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