SPECIOUS SEA SLUGS
Specious: misleading in appearance, superficially plausible but actually incorrect.

Cryptics Mimics Variations & Morphs

Most divers just enjoy their recreation with little exposure to, or even interest in, the scientific process. They take pleasure in what they see and find, often recording those finds on a camera. There comes a time though when many want to put a proper name to the images of those finds. It is only natural to use and rely upon easily identifiable external features to separate species within a family/genus, colours and patterning being to the forefront in this process, as set out in reliable identification and field guides. In fact, there is little else to employ, if external anatomical features are identical, when relying upon an image for a species identification. However, the reliance on colour and pattern in identifying species has recently been demonstrated to have limitations in certain genera, for example, the nudibranchs of the Chromodoris and Felimida genera. 

Same but Different – Different but same
It comes as a huge surprise to interested divers to learn that a specimen of sea slug that looks remarkably like one species is actually another and still more of a surprise to learn that a species itself may have a range of different presentations – variations or morphs. Yet another level of astonishment is reached when they find out that a morph of one species looks convincingly like another species. In plain talk, some that look the same are different species and some that look different are the same species. Interestingly, a colour morph can fall into both of those categories. It looks different to the usual form of the species, but is the same species, but can can look the same as another species, but is not that species. Confronted with this dilemma confusion reigns together with its travel partner, disbelief, but this is not a bad thing. Nothing should be taken at face value. If these morphs are found through science then there has to be a process and evidence to arrive at that conclusion. The process and evidence of original descriptions has given us species and the characteristics that usually enable us to differentiate which species is what. What some of those original descriptions lack is the range or extent of intraspecific variation possessed by the species. In the past most of that information was fleshed out over time and subsequent observation with many flawed assumptions often being made along the way. Back then it seemed reasonable to decide arbitrarily what external differences could be ignored in deciding on an identification. That method is now no longer considered reliable and greater caution is being  observed. The terms cryptic, mimic, variation and morph are used to explain differences and their relationships. It will be seen that they are all interconnected.

Intraspecific Variation
We know that all individuals of a species are not identical and with all species there has long been an accepted level of intraspecific variation. In simplistic terms, this is brought about by an “error” in the DNA replication process of the germ-line cells (those that create egg/sperm cells) giving rise to a mutation that is passed on to offspring. Whether that mutation benefits or disadvantages or is neutral to that offspring is another matter. Care should be taken to be aware of the differences exhibited by different maturity levels in a species population. Sea slugs, being hermaphrodites, do not of course exhibit sexual dimorphism (morphological differences between the sexes not related to reproduction) such as is often observed in fish for example. This variation between individuals of the same species is seen in how they behave, respond to natural selection pressures and what concerns us in this article – their appearance. Most sea slugs show some variation in colour and pattern across the population, usually revolving around a most-common or core presentation such that they are usually recognized as the same species. However, in some sea slug genera colour polymorphism (occurrence of different colour patterns within the one species) can be considerably disparate to the extent that extreme examples can be unrecognisable as that species. This characteristic is becoming more and more realised and researched. Questions therefore are raised about what are the boundaries of intraspecific variation in appearance? When does a difference in appearance, and how much of a difference, heralds a different species? How can that be ascertained?

Example of intraspecific variation – Berthella martensi.
Upper left: Translucent grey with dark brown spots of varying sizes. Upper right: Translucent cream covered with a fine brown reticulation. Lower left: Translucent grey, dark brown spots of varying size, Light brown edging to foot, mantle segments and on oral veil. Lower right: Dark brown all over including rhinophores. Cream spots raised into significant tubercles of varying size and randomly distributed. Perhaps future widespread sequencing will eventually separate these variations into distinct species.

Another example of intraspecific variation – Goniobranchus splendidus.
Upper left: A specimen with port-wine colouration to the dorsal blotches. Rhinophores and gill colour match the port-wine of the dorsum, mantle margin tending to orange as does tail tip. Upper right: Dorsal blotches of an orange hue as are rhinophores and gills. Mantle margin is yellow and tail carries a yellow tip. Lower left: Dorsal markings present as a broken medial line, port-wine in colour, tail with a translucent colourless tip. Lower right: Just to confuse further here is a specimen without any dorsal blotches at all. Rhinophores and gills are port-wine in colour and the mantle margin is bright yellow. The tail carries a translucent colourless tip.

Further examples of intraspecific variation – Phyllidia ocellata.
Here are four variations of the one species: Phyllidia ocellata. Note the variation in tubercle sizes and different arrangement of the pattern and colouration of the ocelli. A large variation in presentation is often associated with a different geographical location.

Cryptic Species – Hiding in plain sight
Not so long ago molecular sequencing of DNA started providing exciting evidence of cryptic species and pseudo-cryptic species✽, the latter of which, concerns us most here. These are not species that are hard to see because they are camouflaged in their habitat, but instead, species that are difficult to recognise because they are camouflaged within another species – externally they look the same or have quite minor differences that were, in the past, considered within the range of that other species’ variability. This revelation caused taxonomists to look even more closely at the internal morphology of specimens to determine those differences. They had the signpost from the genetic testing, pointing to a need for more detailed examinations of digestive and reproductive systems. Those re-examinations found those differences to support the findings of the molecular sequencing. Sometimes fine variations in colour patterning may be ascertained and linked to the pseudo-cryptic species allowing a degree of visual recognition/separation.

A great example of separation of pseudo-cryptic species – Pteraeolidia.
Left: Pteraeolidia ianthina, Nelson Bay, NSW (image courtesy of Terry Farr). Right: Pteraeolidia semperi, Sunshine Coast, Qld. Long considered a single species across all of its Indo-Pacific locations. Molecular sequencing separated out and allocated Pteraeolidia ianthina (left) to central and southern NSW. It presents with only two purple bars to the oral tentacles and a lack of white pigment on head/face. The balance, in all other locations, have been placed in Pteraeolidia ‘semperi’ (right) until additional sequencing can separate into yet more species, as suggested by the initial research. These present with three purple bars to the oral tentacles and a white head/face. Another difference relates to markings on the body-sides, not usually visible in photos.

Hexabranchus sanguineus (the well-known Spanish Dancer), long accepted as a single species, has been found to be a complex of five species after 200 years of taxonomic chaos, including up to fifty names and thirty synonyms. Not only that, but the molecular sequencing has revealed a number of morphotypes within each species further complicated by ontogeny appearance. Pseudo-cryptic species indeed. Above Left: A mature form of Hexabranchus sanguineus – Above Right: A mature form of Hexabranchus lacer.

All this suggests that the traditional morphological methods did not provide sufficient resolution for species delineation in taxonomic research. Also the definition of a species, that is, its boundaries, might have to be reviewed/changed, as too, the cut off (degree of difference) used by taxonomists in analysing molecular data. There is disagreement on where these cutoffs should be placed. Another complicating factor is the so called permeable species boundaries thought to be prevalent in recently diverged taxa.

Mimicry
Mimicry is a complex subject. Here we are concerned with sea slug species visually mimicking one another for defensive purposes rather than items in the habitat or unrelated animals. Mimicry is not a conscious effort by a species to look like another. It is an evolved resemblance that has come about through selective pressure in the habitat. It is the success of those evolved changes in that habitat that sustains the mimic. The mimic is successful because it gains a survival advantage usually in that its appearance serves to warn a predator that it may be noxious or distasteful, just like its model. The mimic may itself be noxious or not. To be a mimic, of course, it should share the same habitat as the model to gain the advantage. There are a number of mimicry categories but two are of particular significance:
Batesian mimicry, this is a bluff, where a non-noxious/non-distasteful mimic is copying the aposematic (warning colouration) appearance of a noxious/distasteful model. This could be called a “parasitic” process. Usually the population level of a Batesian mimic should be considerably lower than that of the model.
Müllerian mimicry, on the other hand, involves two or more species that are all noxious/distasteful and aposematic species, sharing a somewhat common appearance for mutual benefit and is the type that generally concerns sea slugs.

These are not to be considered rigid categories. The toxicity of the members of a Mullerian “group” could all vary significantly even blending into the Batesian level of mimicry. As Behrens, 2005, states: “Batesian and Mullerian mimicry are not mutually exclusive. In fact, they represent two extremes with an array of possible mimics and models between.”

Mullerian mimicry examples
Recent research has uncovered a number of groups of mimics based around certain distinguishing features. The identification of species within these groups is further complicated by intraspecific colour variations and polymorphism. These are a nightmare for field guides.
Above: These four species are representative of a group of Goniobranchus species that have a white notum (sometimes speckled) and marginal mantle bands of various colours, number and arrangement.
Below: Another four Goniobranchus species representative of a group that has a red reticulation of various presentation over a white notum.

The mimicry may not be perfect. It may be that the mimic is evolving towards the perfect look. Also, only certain traits may be necessary to deceive a predator and we, as humans, may perceive the mimicry different to how a predator perceives it. Perhaps the mimic may be imitating several models in the habitat.

On the east coast of Australia (central to southern) there is a group of what Dr Bill Rudman has called “the red-spotted chromodorids”. These all exhibit a red-spotted colour pattern on their notum being aposematic or warning colouration. It is believed that by doing so they all promote the warning and thus share the load of educating predators as to the disadvantage of attacking them and encountering the noxious mantle glands they all possess. There are several other red or dark-spotted species throughout the Indo-Pacific and although in different habitats, and cannot be considered mimics, serve to show that this form of warning colouration is widespread and probably effective perhaps in providing a generic visual signal able to be perceived by predators.

Mullerian mimicry examples
Clockwise from upper left: Goniobranchus daphne, Goniobranchus splendidus, Goniobranchus tasmaniensis (Image courtesy of Terry Farr) & Mexichromis festiva. Four species, representative of a larger group, found on the central to southern east coast of Australia, having a white notum with red spots/blotches. By having a similar in appearance they all serve to share the load of “teaching” predators of the presence of noxious mantle glands. Some have a wider distribution than others.

The problem experienced by many sea slug enthusiasts in separating many species of the phyllidiids just serves to highlight the use of mimicry within the family. Predators are faced with the same dilemma. The colours, the tubercles and their arrangements are all along the same theme and differentiation is difficult, thus, all supporting each other to advertise unpalatability. There are also species in other genera of nudibranchs that exhibit an appearance similar to the phyllidiids, such as Goniobranchus geometricus and some species of Denrdrodoris, and no doubt, reaping the anti-predator benefit.

Above: The Phyllidiidae family is well known for the similarity in appearance among many of its members, leading to frustration in identification. With so many looking much the same it points to the success of the model. There is no doubt they are all examples of Mullerian mimicry and so too are some non-phyllidiids. A couple are illustrated here, making the most of the protection afforded by mimicking those noxious models. Clockwise from top left: Phyllidiella pustulosa, Phyllidia elegans, Goniobranchus geometricus and a juvenile Dendrodoris carbunculosa.

Morphs
In its strictest application the technical description of morphotypes of a species is complicated. One of the requirements though is that the morophotypes must occupy the same habitat together at the same time, that is, not be a geographical variation. However, the term morphs (or morphotypes) is applied here loosely, as a different presentation of the one species regardless of location, just as it is used in most of the literature and many references. Morphs are a particular type of intraspecific variation, a recognized consistent form not a random or a graded variation in appearance. Morphotypes of certain sea slugs have been found to mimic the appearance of other species of the same genus where that other species is abundant in the region. Mostly these are found in regions where the most typical appearance (“normal type”) of the mimic species is not found (i.e. extending their range) – a geographically-based variation. However, in some instances a different morphotype again has been found in the same region together with its “normal type”. The suggested methods by which these morphotypes arise include hybridisation and introgression associated with semi-permeable species boundaries, processes for discussion in a later NudiNote.

Morphotype example
Left: The “typical” originally described presentation of Chromodoris joshi (image taken in Philippines). Right: A morphotype of Chromodoris joshi mimicking Chromodoris magnifica (image taken at the same site in Philippines). This specimen matches the presentation of a specimen proven to be a genetic match to Chromodoris joshi in the Philippines. Molecular sequencing has also revealed yet another morphotype of Chromodoris joshi mimicking Chromodoris magnifica in Western Australia. Interestingly, it has been discovered that there are only a few (as little as one to four) mutational steps necessary for the variations.

A single species can fit into all of the categories we have discussed, for example, when a species morph, being a type of intraspecific variation, chances to mimic the appearance of a locally abundant congeneric it can become pseudo-cryptic within that population.

Like all good science these recent studies identifying cryptics, mimics, variations and morphs although supplying some answers create yet more questions.

What does all this mean for recreational divers wanting a name to put to their images, but having “unreliable” colour patterns to contend with? Reliable, up to date field guides are a good start, but necessarily limited in the number of variations and explanations they are able to include. Where some species look remarkably similar, refer to the geographical location for some possible differentiation. Finally, “If it looks like a duck, walks like a duck and quacks like a duck …..”  After all, who is going to tell you that you are wrong from just viewing an image.

✽ – Cryptic species are defined as appearing the same, being morphological indistinguishable, but exhibiting considerable genetic divergence. (It may transpire that these species may eventually be distinguishable when new methods of morphological examination and refinement of the definitions used are developed.)
 – Pseudo-cryptic species are defined as appearing the same, though morphological distinguishable under fine examination and exhibit considerable genetic divergence.
 – The use of the terms quasi-cryptic, semi-cryptic & false-cryptic are fine distinctions not necessary for the scope of this article.

David A. Mullins – November 2023

References:
– Rudman, W. B. (1991). Purpose in pattern: the evolution of colour in chromodorid nudibranchs. Journal of Molluscan Studies. 57, 5–21.

– Edmunds, M. (2000). Why are there good and poor mimics? Biological Journal of the Linnean Society; 70: 459-466.

– Gosliner, t. M. (2001).Aposematic coloration and mimicry in opisthobranch mollusks: new phylogenetic and experimental data. Bollettino Malacologico, Roma, 37 (5-8): 163-170.

– Sherratt, T. N. (2002). The coevolution of warning signals. Proceeding of the  Royal Society London, B 269, 741–746.

– Sherratt, T. N. (2002). The evolution of imperfect mimicry. Behavioral Ecology Vol. 13 No. 6: 821–826.

– Rudman, W. B.  (2004, July 23). Mimicry – red-spotted chromodorids. [In] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/factsheet/redspot and associated messages.

– Rudman, W. B. (2004, July 23) Mimicry. [In] Sea Slug Forum. Australian Museum, Sydney. Available from http://www.seaslugforum.net/factsheet/mimicry and associated messages.

– Behrens, D. W. (2005) Nudibranch Behaviour. New World Publications, Florida, USA.

– Harper Jr, G. R. & Pfennig, D. W. (2007). Mimicry on the edge: why do mimics vary in resemblance to their model in different parts of their geographical range? Proceedings of the Royal Society B; 274, 1955-1961.

– Sherratt, T. N. (2008). The evolution of Müllerian mimicry. Naturwissenschaften 95:681–695.

– Speed, M. P. & Ruxton, G. D. (2010). Imperfect Batesian Mimicry and the Conspicuousness Costs of Mimetic Resemblance. The American Naturalist Vol. 176, No. 1.

– Cortesi, F. & Cheney, K. L. (2010). Conspicuousness is correlated with toxicity in marine opisthobranchs. Journal of Evolutionary Biology. 22 1509-1518.

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– Wilson, N. G. & Burghardt, I. (2015). Here be dragons – phylogeography of Pteraeolidia ianthina (Angas, 1864) reveals multiple species of photosynthetic nudibranchs (Aeolidina: Nudibranchia). Zoological Journal of the Linnean Society, 2015.

– Wilson, N. G., Winters, A. E., Cheney, K. L. (2016). Tropical Range Extension for the Temperate, Endemic South-Eastern Australian Nudibranch Goniobranchus splendidus (Angas, 1864). Diversity 2016, 8, 16.

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– Padula, V., Bahia, J., Stöger, I., Camacho-García, Y., Malaquias, M. A. E., Cervera, J.L. & Schrödl, M. (2016). A test of color-based taxonomy in nudibranchs: molecular phylogeny and species delimitation of the Felimida clenchi (Mollusca: Chromodorididae) species complex. Molecular Phylogenetics and Evolution. 103, 215–229.

– Layton, K. K. S., Gosliner, T. M. & Wilson, N. G. (2018). Flexible colour patterns obscure identification and mimicry in Indo-Pacific Chromodoris nudibranchs (Gastropoda: Chromodorididae). Molecular Phylogenetics and Evolution; 124: 27–36.

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– Winters, A. E., Wilson, N. G., van den Berg, C. P., How, M. J., Endler, J. A., Marshall, N. J., White, A. M., Garson, M. J. & Cheney, K. L. (2018). Toxicity and taste: unequal chemical defences in a mimicry ring. Proceeding of the  Royal Society London, B; 285: 20180457.

– Gosliner, T. M., Valdés, Á., and Behrens, D. W. (2018). Nudibranch & Sea Slug Identification: Indo-Pacific – 2nd Ed. New World Publications: Jacksonville, FL.

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– de Solan, T. & Aubier, T. G. (2019). The Evolutionary Importance of Cues in Protective Mimicry. Frontiers in Ecology and Evolution. Vol. 7; Article 283.

– Takahashi, Y. & Noriyuki, S. (2019) Colour polymorphism influences species’ range and extinction risk. Biological Letters; 15: 20190228.

– Golestani, H., Crocetta, F., Padula, V., Camacho-García, Y., Langeneck, J., Poursanidis, D., Pola, M., Yokes, M. B., Cervera, J. L., Jung, D.-W., et al. (2019). The little Aplysia coming of age: From one species to a complex of species complexes in Aplysia parvula (Mollusca: Gastropoda: Heterobranchia). Zoological Journal of the Linnean Society; 187, 279–330.

– Soong, G. Y., Wilson, N. G. & Reimer, J. D. (2020). A species complex within the red-reticulate Goniobranchus Pease, 1866 (Nudibranchia: Doridina: Chromodorididae). Marine Biodiversity (2020) 50:25.

– Layton, K. K. S., Carvajal, J. I. & Wilson, N. G. (2020). Mimicry and mitonuclear discordance in nudibranchs: New insights from exon capture phylogenomics. Ecology and Evolution. 2020;00:1-17.

– Gosliner, T. M. (2020). Sleuthing cryptic Chromodorids (Mollusca, Nudibranchia): adding to Philippine marine biodiversity. Philippine Journal of Systematic Biology. Volume 14 Issue 2.

– Feliciano, K., Malaquias, M. A. E., Stout, C., Brenzinger, B., Gosliner, T. M. & Valdes, Á. (2021). Molecular and morphological analyses reveal pseudocryptic diversity in Micromelo undatus (Bruguiere, 1792) (Gastropoda: Heterobranchia: Aplustridae). Systematics and Biodiversity; 19(7): 834–858.

– Soong, G. Y., Bonomo, L. J., Reimer, J. D. & Gosliner, T. M. (2022). Battle of the bands: systematics and phylogeny of the white Goniobranchus nudibranchs with marginal bands (Nudibranchia, Chromodorididae). ZooKeys 1083: 169–210.

– Tibiriçá, Y., Pola, M., Pittman, C., Gosliner, T. M., Malaquias, M. A. & Cervera, J. L. (2023). A Spanish dancer? No! A troupe of dancers: a review of the family Hexabranchidae Bergh, 1891 (Gastropoda, Heterobranchia, Nudibranchia). Organisms Diversity & Evolution. Published online: 20 June 2023, https://doi.org/10.1007/s13127-023-00611-0

– This NudiNote has been modified from two previously published articles in Dive Log Australasia Magazine – NudiNotes Column, Issue: #401 (August 2023): pp. 20-21 and  Issue: #402 (October 2023): pp. 20-21 by David A. Mullins.

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