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Aposematic (warning) coloration & Batesian mimicry


Defenses of nudibranchs and their relatives include aposematic (warning) coloration & Batesian mimicry, considered in 2 sections below, and

, considered in other sections. 

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Research study 1

photograph of aeolid nudibranch Hermissenda crassicornis
drawing of tip of ceras of Hermissenda crassicornis showing disposition of pigment areasAn individual aeolid Hermissenda crassicornis may have several hundred cerata.  Each, when mature, bears a cnidosac containing several thousand undischarged nematocysts. Brightly demarcated orange and white bands demarcate the location of the cnidosacs in Hermissenda, and orange and blue markings adorn the dorsal part of the body, with white piping on the rhinophores and oral tentacles. Similar colorful markings are exhibited by other aeolids.  It is generally accepted that these are examples of aposematic1 coloration, that is, a warning to a nudibranch’s predators about the presence of something unpleasant.  An aeolid will often “bristle” or wave its cerata about when irritated, perhaps making itself appear bigger or, a propos of the defensive function being considered in this section, offering a warning display of something noxious.  In theory, a naive predator takes a mouthful of cerata, gets stung and, on later contact with an individual of the same species, remembers the experience and does not bother it again.  For warning or aposematic coloration to work, the predators have to be daytime visual hunters with good colour vision.  This restricts the field to fishes, crustaceans2, and birds (the last in shallow subtidal and intertidal areas).  Although convincing experiments3 on aposematic coloration in nudibranchs are lacking, it is hard to ignore an apparent convergent evolution of possible warning drawing of ceras of an aeolid nudibranch Eubranchus to show location of ceratal glandscoloration4 seen in many aeolids.  Drawing from Bürgin 1965 Veliger 7: 205.

NOTE1 lit. “away signal” G., referring to bright, easily visible colours displayed by toxic animals (and some plants) that convey a “do not eat, for I am unpalatable, and will make you sick” message to predators with colour vision.  A familiar example of aposematic colouration is the black and yellow markings on bees and wasps

NOTE2 learning ability in crustaceans is poorly developed, or at least is not evident in the kinds of experiments used to test for it

NOTE3 by feeding Hermissenda on non-nematocyst-bearing food, such as tunicates, it is possible to eliminate all nematocysts from the cerata through routine cycling of these in the cnidosacs. As a possible research project, couldn't these nematocyst-free specimens now be tested with experienced and naive predators, such as cottid fishes, to test the efficacy of the nematocyst defenses, learning in the predator, and putative aposematism? This has been tried elsewhere, with inconclusive results, but appears not to have been investigated in west-coast species

NOTE4  although this section deals with warning coloration associated with cnidosacs within the cerata of west-coast aeolids, studies on other aeolids, such as Eubranchus spp. in Europe, reveal that ceratal glands of unknown function may also be present (see drawing on Right).  For example, when a ceras of Eubranchus is is pinched, these glands release a white secretion.  It the secretion is defensive, then warning coloration on the cerata could be associated with it, with nematocysts, or with both. There are several west-coast species of Eubranchus to experiment on. Edmunds 1966 J Linn Soc Lond (Zoology) 46: 27

Research study 2

photograph of cerata of aeolid Hemissenda crassicornisColours in nudibranchs are created by pigment, both in the epidermis and in the digestive-gland diverticula, and by structure, where light is diffracted through granules contained in vacuoles in special cells of the epidermis.  Studies on colour patterns of Hermissenda crassicornis at Scripps Institution of Oceanography, La Jolla, California reveal that the bright orange coloration is from fat-soluble carotenoid pigments in epidermal cells. 

drawing of cross-section through gastrodermis of aeolid nudibranch Hermissenda crassicornis showing pigment cellsColours of the digestive diverticula, easily seen through the transparent skin, may be brown, ochre, or reddish, partly owing to the type of food being eaten and partly to the presence of pigment-bearing vacuole cells among the digestive and glandular cells in the gastrodermis of the diverticula (see diagram on Left). These pigmented vacuole cells are usually brown, and their colour is less dependent upon the type of food being eaten. 

cross-sectional view of epidermis of ceras of aeolid nudibranch Hermissenda crassicornis showing white granules colour cellsThe bright structural colours of blue, white, and yellow in Hermissenda are caused by diffraction of light passing through granules within the epidermis followed by differential absorption of the wavelengths emitted.  Apparently, the granules in different parts of the body differ in chemical composition, and this produces the different shades of blue and yellow. Where the granule cells are mixed, as in the piping along the tail, the resulting colour is white.  The blue piping in Hermissenda is quite striking, especially where it forms the 2 unusual rhomboidal outlines, one just posterior to the rhinophores, and the other outlining the heart/pericardium and in the centre part of the tail.  Bürgin 1965 Veliger 7: 205.

NOTE colours in H. crassicornis vary geographically, especially with respect to the extent of white at the tips of the cerata and blue in the pipings

Research study 3

Discussion of aposematic coloration in opisthobranchs is hampered by not knowing their predators and, thus, not knowing the extent to which vision plays a role in hunting and capture. One confirmed predator of nudibranchs, the cephalaspidean Navanax inermis, hunts by chemotactile means and has only tiny eyes with no visual resolution. Also, potential visual predators, like fishes and crustaceans, may use a portion of the ultraviolet part of the light spectrum to identify their prey. In short, what looks brightly coloured to our eyes may appear quite different to a crab or fish on the hunt for prey. Aeolid nudibranchs appear to our eyes to be more brightly coloured than dorids, yet aeolids lack the repertoire of defenses (skin chemistry, spicules, acid) present in many dorids. It would be interesting to know the proportion of dorids that do NOT contain secondary metabolites, but unfortunately there are no statistics kept on such negative data. One author proposes 4 criteria that must be met to justify a certain organism being considered to be aposematic.  It must be brightly coloured, be unpalatable to some predators, be avoided by some predators because of its colours, and be better protected than comparable cryptic species.  Edmunds 1966 J Linn Soc Lond (Zoology) 46: 27; see also Edmunds 1987 Amer Malacol Bull 5: 185 and Edmunds 1991 Malacologia 32: 241.

NOTE of crustaceans, only tropical mantid shrimps are known to see in ultraviolet

NOTE this same author, after reviewing protective mechanisms in aeolid nudibranchs up to 1966, concludes that there is "no evidence" for the presence of warning coloration in aeolids. However, more recently, other "nudibranchologists" have adopted a "brighter" outlook on the subject. West-coast scientists interested in this subject as relating to nudibranchs and nematocyst defenses may find the following articles of interest:  Aguado & Marin 2004 J Moll Stud 73: 23 - field and laboratory tests with a Spanish aeolid Cratena peregrina using live individuals and models exposed to potential fish predators; design may have problems in that possible toxic secondary metabolites are not accounted for.  Edmunds 2009 J Moll Stud 75: 203 – further background material on nematocyst defense in aeolid nudibranchs

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Batesian mimicry
Research study 4

Given that the secondarily acquired nematocysts in aeolids are defensive, and assuming that the bright colours of the aeolids are aposematic, the next question to ask is are there any mimics? That is, are there animals that are otherwise palatable but have evolved colour, shape, and behaviour to mimic those of a toxic model? These are known as Batesian mimics and, while their existence is well documented in insects such as butterflies and moths, they are essentially unknown among marine invertebrates.  The mimic is recognised by a potential predator as something not good to eat, and thus gains a measure of protection.  The next “order” of mimicry is Mullerian mimicry, where several unrelated but toxic prey organisms evolve similar warning signals, thus sending a common message to potential predators.  The best example from the terrestrial world is the evolution of orange/black/yellow coloration in wasps, ants, and lepidopterans (both larvae and adults), which sends a common “don’t eat” message to potential predators.  In simple terms, it makes it easier for the predator to remember what not to eat.  Keep in mind that the predators involved in terrestrial examples of Batesian and Mullerian mimicry are thought to be mainly birds, with high-resolution, good colour-vision eyes, and good memory.  As noted in Research Study 3 above, the only known predators of opisthobranchs are other “sightless” opisthobranchs that hunt by chemotactile means.  Those who write about mimicry in opisthobranchs understandably tend to be cautious, though optimistic. The problem, once again, is in devising experiments to demonstrate that a certain colour or pattern is: 1) functioning as warning, and 2) being copied by another organism.  A good review of world literature on the topic can be found in Gosliner & Behrens 1990 p. 127 In, Adaptive Coloration in Invertebrates (Wicksten, compiler) Texas A&M Univ Press; see also Gosliner 2001 Bollettino Malacologico, Roma 37: 163 for field tests of aposematic coloration and mimicry in species of Flabellina and Chromodoris in Papua New Guinea.

NOTE the several references in the literature to marine animals resembling one another, usually one with known toxic or otherwise unpalatable properties and one without (or at least not known), are placed in this "unknown" category until suitable experiments are done. Some of these pairings are quite convincing, as shown by the examples in Research Study 5 below; others, less so

Research study 5

photographs of aeolid nudibranch Flabellina iodinea and its purported Batesian mimic amphipod Podocerus cristatus courtesy Jeff Goddard, Santa Barbara, Californiaphotographs of aeolid nudibranch Flabellina trilineata and its purported Batesian mimic amphipod Podocerus cristatus courtesy Jeff Goddard, Santa Barbara, CaliforniaOn the west coast there are 2 striking examples of convergent colour patterns in nudibranchs and amphipod crustaceans that could represent Batesian mimicry. The first involves Flabellina trilineata and its remarkable look-alike amphipod Podocerus cristatus (35mm and 5mm in length, respectively) collected from Cape Arago, Oregon (see photos on Left). In this area both purported mimic and model inhabit the same rock overhangs and cobble areas. The similarity of the 2 organisms is quite striking, with the white antennae of the amphipod resembling the white cephalic tentacles and rhinophores of the nudibranch, and the red-orange pigment spots on Podocerus resembling the cerata clusters of Flabellina.

A second example of aeolid-amphipod look-alikes concerns Flabellina iodinea and the same amphipod Podocerus cristatus, this time from San Luis Obispo, California (photos on Right). Given that the amphipod is truly one and the same species, it is remarkable that selection favours one mimicking pattern in one area, and another pattern not so far distant. Some colours in crustaceans are skin pigments and fixed, while others are contain in chromatophores and are adjustable, so it would be interesting to know how morphologically labile are the pigments in Podocerus.

As most amphipods are edible to fishes, the scientist who assembled these photos at the site listed below suggests that the resemblance may indeed be an example of Batesian mimicry, where a palatable organism (the amphipod) gains protection from its predators by mimicking an inedible or repugnant organism (the nudibranch). All that is needed now is to find enough of each species to do some experiments with naive and experienced fishes. Goddard 1984 Shells & Sea Life 16: 220. Photos courtesy Jeff Goddard, Santa Barbara, California, Todd Huspeni, Mike Behrens, and seaslugforum.

Research study 6

map showing distribution of different colour patterns of amphipods Podoceros cristatus at different locations latitudinally along the west coast of North AmericaA later paper adds some new material to this fascinating account of potential Batesian mimicry between aeolid nudibranchs and the amphipod Podocerus cristatus. The author notes that while no experimental evidence exists to support the mimicry, a body of photographic documentation of colours and colour-pattern resemblances between aeolid nudibranchs and Podocerus is accumulating that is hard to resist. Note in the accompanying photographs that the amphipods tend to resemble in colour pattern the species of aeolid nudibranch Flabellina (also another species Noumeaella rubrofasciata) that is common in a given latitudinal area along the west coast. One requirement of Batesian mimicry is that the participant species live in close proximity such that potential predators, such as fishes, experience close contact with them both. As the author notes, and two of the photographs appear to attest to, it is not uncommon for the amphipods to crawl about in the open within a few cm distance of their purported toxic models. Goddard 2015 Mar Biodiversity 25 Sept: 1-3.

NOTE this is not surprising, as neither species may be common enough in any area to enable experimental collections to be made. The answer may lie in breeding experiments. Rear up both species including selective crosses of different-coloured Podocerus, present them alone and together with aeolids Flabellina spp. to naive and experienced fish predators, and record predatory strikes by the fishes

NOTE underwater photographers are not averse to manipulating their subjects for best appearance, and this has to be monitored by an experimentor. This is a good time to appeal to west-coast underwater photographers for their help: if you have photographs of Podocerus with or without aeolids and would like to get involved with this interesting research project, send the images either to the ODYSSEY or to Dr. Jeff Goddard with information on location, depth, date, habitat and, additionally, any aeolids that may be nearby

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So, all of this is interesting, but let's take a moment to check our understanding of warning coloration and mimicry as presented in the following statements. Some are true or at least have the possibility of being true, some are false, and others are given simply to promote discussion. When you are ready, CLICK HERE to see explanations, which themselves may be open to discussion.

The distinctive colour patterns of the amphipod are not examples of Batesian mimicry; rather, they warn of the amphipod’s own toxicity to potential predators (i.e., warning or aposematic coloration).

The amphipod is not a Batesian mimic of the nudibranch; rather, it is the reverse, the nudibranch is a Batesian mimic of the amphipod.

The relationship is not Batesian mimicry but, rather, an example of Mullerian mimicry.

There is no mimicry being demonstrated. The amphipod’s colours serve for cryptic camouflaging (such as pattern disruption) and resemblance to patternings of the nudibranch are coincidental.

The tiny size of the amphipod Podocerus cristatus (3-5mm) makes it unlikely to be a mimic of the much larger (20-40mm) aeolid nudibranch Flabellina spp.

One requirement of Batesian mimicry is that the organisms be out and about at the same time, and visible to potential predators. How can this be true for Flabellina spp. that are mostly nocturnal, and for Podocerus cristatus that crawls about deep in its algal foodstuffs?

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