Research Study 1

Fig. 1. Brown pigment cells in digestive-diverticulum gastrodermal cells in Hermissenda crassicornis

Fig. 2. Blue lines over the heart and on the tail of Hermissenda crassicornis

Fig. 3.  Location of white granule cells in the skin of Hermissenda crassicornis

Colours 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.  Colours 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 (Fig. 1). These pigmented vacuole cells are usually brown, and their colour is less dependent upon the type of food being eaten. The 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. The blue piping in Hermissenda is quite striking, especially where it forms the two unusual rhomboidal outlines, one just posterior to the rhinophores, and the other outlining the heart/pericardium and in the centre part of the tail (Fig. 2).  Where the granule cells are mixed, as in the piping along the tail, the resulting colour is white (Fig. 3).

NOTE  interpretation of the study is extra-challenging in that the illustrations are presented in black-and-white.  No colour plates are included in the original.  The author states that 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, but no visual support for this, as noted, is provided

Research Study 2

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 this type of negative data. One author proposes four 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. 

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 (field and laboratory tests with a Spanish aeolid Cratena peregrina using live individuals and models exposed to potential fish predators, although the design of the experiments may have problems in that possible toxic secondary metabolites are not accounted for), and Edmunds, 2009 (further background material on nematocyst defense in aeolid nudibranchs)

Research Study 1:     Batesian & Mullerian mimicry

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, and known for certain tropical fishes, 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 good colour-vision, high-resolution eyes, and good memory.  As noted in another section of the ODYSSEY, one common predator of opisthobranchs is a “sightless” opisthobranch Navanax inermis that hunts 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); see also Gosliner (2001) 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 3 below; others, less so...more in the "wishful-thinking" category

Research Study 2:     Batesian & Mullerian mimicry

Fig. 1.  Nudibranch Flabellina trilineata and possible Batesian look-alike amphipod Podocerus cristatus

Courtesy Jeff Goddard, Santa Barbara, California

Fig. 2.  Nudibranch Flabellina iodinea with Batesian look-alike Podocerus cristatus

Courtesy Todd Huspeni & Mike Behrens, and seaslugforum

On the west coast there are two 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 (Fig. 1).  In this area both purported mimic and model inhabit the same rock overhangs and cobble areas. The similarity of the two 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 (Fig. 2).  Given that the amphipod is truly one and the same species (in the photographs the amphipods featureed seem to be quite different), it is remarkable that selection favours one mimicking pattern in one area, and another pattern in another area not so far distant, suggesting some sort of commonality in predators.  Some colours in crustaceans are skin pigments and fixed, while others are contained 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 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 - ones that might be willing to eat both types of "prey". 

Research Study 3:     Batesian & Mullerian mimicry

Fig. 1.  Examples to date of nudibranch/amphipod pairings in different geographical locations that may represent Batesian mimicry

Courtesy Jeff Goddard, Gary McDonald, Allison Vitsky, Alicia Hermisillo

A later publication adds some new and perhaps more convincing 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 photographs in Fig. 1 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 visible 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 short (few cm) distance of their purported toxic models.

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 a researcher.  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, specific aeolids that may have been seen nearby

Research Study 1:     Mullerian mimicry

Fig. 2.  Top: cnidosac morphology of Flabellina goddardi showing its distinctive sub-apical orange-red band at the distal end of the digestive-gland diverticulum.   Bottom: squash preparation of a cnidosac of F. goddardi showing a nematocyst complement (microbasic euryteles) characteristic of its favoured Bougainvillia-like prey hydroid

Fig. 1.  Possible Mullerian mimics Flabellina goddardi and F. trilineata

Courtesy Jeff Goddard and Douglas Klug, California

Mullerian mimicry is a type of mimicry where similar colour patterns are found in species that are known to be toxic, presumably arising from convergent evolution.  An example may be a species-pair (Fig. 1) of Flabellina aeolids in southern California. The two, Flabellina goddardi and F. trilineata, are similar in size, cerata morphology, presence of lengthwise white body stripes, and cnidosac coloration (Fig. 2).  Some differences are present, including single versus triple white striping, and coloration and shape of oral tentacles and rhinophores.  Both species eat hydroid polyps.  The authors present photos of two other world species of aeolids with similarly strikingly orange-coloured cerata (not shown here), and suggest a possible Mullerian mimicry-type worldwide complex relating to warning coloration. The predators being defended against would likely be fishes with their good colour vision. The commonality of the orange coloration of the cerata suggests that it transmits well through seawater.  Certainly the human eye is sensitive to these wavelengths, although it should be noted that at any but shallow depths they would appear black, owing to differential absorption of red wavelengths, in particular, with increasing depth in seawater. 

NOTE in addition to the rhinophore colour differences mentioned here, some subtidal specimens of Flabellina goddardi may have white lines on the posterior aspects of their rhinophores.  However, let's get real...this is NOT rocket science!  No potential predator, good vision or not, is going to count lines or check for minute colour differences.  It will be a visual blast of colour that a predator will see, accompanied by quick attack or withdrawal

NOTE there is a growing literature on colour sensitivity in the eyes of tropical fishes, most notably an ability to sense wavelenghs in the ultraviolet portion of the colour spectrum, something that could repay further research on warning coloration in aeolid nudibranchs