Why slugs are more interesting than you think

It’s probably fair to say that slugs are not the most well loved of animals. To most people these gastropods are dull coloured, slimy and unattractive, to gardeners they’re a sworn enemy. While this might be true of typical garden, or land, slugs, there is another group of slugs that are in an altogether different league. The marine slugs, or Opisthobranchia, are a little known group comprising some 5000 to 6000 species of beautifully coloured animals, many of which possess fascinating biological adaptations that are either unique or exceptionally rare in the animal kingdom.

Glaucus atlanticus is a Nudibranch belonging to the superfamily Aeolidoidea. Like other members of this group it is able to feed on venomous Cnidarians such as the Portuguese man o’ war, Physalia physalis. Uniquely amongst animals nearly all aeolid slugs are able to store the stinging cells of their prey, cnidocytes, for use in defense.

Take for example, Glaucus atlanticus. This species, which is found throughout the world’s tropical and temperate seas, is immune to the stinging cells of Cnidarians (jellyfish and related species) called Cnidocytes. This means that despite being only 3cm long it is able to feed on dangerous and highly venomous Cnidarian species including the Portugese man o’ war, Physalia physalis, and the the by-the-wind-sailor, Velella velella.

That would be impressive enough on its own, however, G. atlanticus goes further by storing Cnidocytes taken from its prey for later use against would-be attackers. Quite how it does this is not yet known. The sting of a Cnidocyte cell is fired when a hair-trigger, called the Cnidocil, is released. These cells can only be used once yet somehow G. atlanticus is able to consume its Cnidarian prey without causing its victims’ Cnidocyte cells to fire. One possibility, supported by studies of closely related species such as Aeolidia papillosa, is that mucus secreted from glands in the oral tube may be what is responsible for preventing the Cnidocytes from firing. Another possibility is that only immature Cnidocytes are stored while mature ones are digested. Alternatively, it may be that the Cnidocyte cells and the slug become acclimatised to one another in the same way that anemones become acclimatised to anemone fish. Whatever the mechanisms behind it, it is impossible not to admire the impressive suite of adaptations possessed by G. atlanticus and its relatives.

It may not be as colourful as other marine slugs but Elysiella pusilla can incorporate functional chloroplasts from its algae diet into its own cells giving this species the ability to photosynthesis and a green colour.

Another group of marine slugs, belonging the clade Sacoglossa, may not have the same striking appearance as G. atlanticus and its relatives but what they lack in appearance they make up for with an adaptation that is found in no other animal group. Sacoglossan slugs, such as Elysiella pusilla pictured above, feed on algae by piercing algal cells with their toothy radula and sucking out the contents. While the cytoplasm of these cells is digested the chloroplasts are retained, intact and functional, within distinct branches of the digestive gland, here they may be stored from hours to months depending on the species. This phenomenon, which falls somewhere between endosymbiosis and predation, has been termed “kleptoplasty”. The chloroplasts within the slug continue to actively photosynthesise and so provide the slug with nutritional benefits. Experiments in the lab have shown that some Sacoglossan species can survive for an impressive ten months without food. Sacoglossan slugs are not the only animals that benefit directly from the photosynthesis of algae, most notably corals live in symbiosis with a type of algae called zooxanthellae which is retained within coral tissues providing them with nutrients in exchange for protection. However, only the Sacoglossan slugs are able to extract and use just the chloroplasts from algal cells while digesting the rest. This is cannot be called a symbiotic relationship since only the slug benefits.

It is interesting to consider how an adaptation like kleptoplasty could have evolved. Heike Wägele and Annette Klussmann-Kolb, writing in the journal Frontiers in Zoology, suggest that initially the uptake and storage of algal cells or chloroplasts, by turning the animals green, provided them with enhanced camouflage. This short-term storage of chloroplasts allowed for a continuation of photosynthesis within the slug and so also provided nutritional benefits. From these humble beginnings the evolution of photosynthesis as an adaptation began. Those animals that could retain chloroplasts in a functional state for extended periods of time would have had the advantage of being able to survive for longer without food. This trait would have been favoured by natural selection and so, once the process had started, evolution would have continued along the path to greater and greater efficiency at photosynthesis.

More recently Katharina Händeler and her colleagues, writing in the same journal, suggested that kleptoplasty evolved in two steps. First was the loss of the ability to rapidly digest chloroplasts, this benefited the slugs in the short-term by providing them with nutrients from photosynthesis. In the second step the slugs evolved the ability to prolong the survival of their acquired chloroplasts by supplying them with the nutrients and enzymes they require to function. In most cases the genes needed to produce these nutrients are contained within the DNA of the algae but not that of the slug. However, in at least the species Elysia chlorotica, and possibly others, algal genes have been incorporated into the slug genome by horizontal gene transfer. The transfer of genes between distinct species is extremely rare amongst eukaryotes and especially so amongst animals. The only known case of horizontal gene transfer from a alga to an animal ocurred in the Sacoglossan lineage, this exceptionally rare event gave species such as E. chlorotica the ability to substantially prolong the life of the chloroplasts it carries and so substantially enhance its fitness.

The bright colouration of Hypselodoris tricolor serves to warn predators that this species is toxic and such not be eaten.

The trait that most defines the Opisthobranchs, or at least the Nudibranch clade, is undoubtedly their extraordinary colouration. This serves to warn would-be predators that these animals are toxic and should not be eaten. As an example of this point, there is a case, in 1937, of a 40 year old man who ate Aplysia kurodai and suffered from severe liver damage, almost certainly as a result of the toxins this species carries.

While some Opisthobranch species are able to synthesise toxic compounds de novo, most acquire them from their diet of other toxic species such as sponges, algae, jellyfish and tiny animals known as bryozoans to which they are immune. These toxins are then stored in specialized glands which surround the mantle called mantle dermal formations, or MDFs. As is so often the case in evolution, a structure that once served a different purpose has been modified to serve a new one. MDFs, it is thought, evolved from former excretory and detoxification organs.

I hope I have convinced you that slugs, of the marine variety, are more interesting than you thought they were. In case I have not there is one more point to consider. The Opisthobranchs are far mor diverse in terms of their colouration and defensive and foraging strategies than almost any other lineage of gastropod. Why should this be so? Well, if Wägele and Klussmann-Kolb are correct it is the reduction and loss of the shell that is responsible for the incredible diversity of Opisthobranch species.

Shells unquestionably provide substantial protection against predators, their loss in the Opisthobranch lineage must then have conferred even greater benefits or this trait would not have evolved. One possibility is that without having to carry a cumbersome and heavy shell around Opisthobranchs were able to exploit new, previously inaccessible, habitats. For example slugs in the Clade Aeolidoidea are able to feed on fragile hydrozoans, a food source that is inaccessible to most other invertebrates. New lifestyles also became accessible for example, with no shell to block the light Sacoglossan slugs were able to take up chloroplasts and use them to photosynthesise.

Without a shell for defense Opisthobranchs have had to evolve novel defensive strategies. Amongst gastropods defensive structures such as the storage of Cnidocytes and toxins are found only in shell-less slugs. These structures are likely to have evolved as a direct result of, and in synchrony with, the reduction of the shell over evolutionary time. This in turn led to the evolution of bright warning colouration such as that seen in Hypselodoris tricolor shown above.

Whatever the exact causes leading to shell loss were, it appears to have resulted in an adaptive radiation as a multitude of new niches suddenly became available. The loss of shells led ultimately to the evolution of a diverse and beautiful group of animals, many of which possess traits which are unique in the animal kingdom. I hope you will agree, that is interesting!

                                                           

Haber M., Cerfeda S., Carbone M. et al. (2010). Coloration and Defense in the Nudibranch Gastropod Hypselodoris fontandraui, Biological Bulletin, 218 (2) 181-188. PMID:
Händeler K., Grzymbowski Y.P., Krug P.J. & Wägele H. (2009). Functional chloroplasts in metazoan cells – a unique evolutionary strategy in animal life, Frontiers in Zoology, 6 (1) 28. DOI:
Wägele H. & Klussmann-Kolb A. (2005). Opisthobranchia (Mollusca, Gastropoda)–more than just slimy slugs. Shell reduction and its implications on defence and foraging, Frontiers in Zoology, 2 (3) DOI:

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