For the most part, land slugs are unprepossessing critters. Inconspicuous in colour and habit, they mostly come to our attention for all the wrong reasons. There’s nothing worse than finding a pile of slug droppings in a half-eaten salad or discovering that yesterday’s plantings in the garden have been demolished overnight by a horde of slimy marauders.
Slugs in the sea are an entirely different proposition. They are bigger, gaudily coloured and bedecked with delicate appendages. Of course, below a few metres’ depth in the ocean colours disappear, so without a light their splendour is not apparent. But to divers, who regularly encounter sea slugs, they are among the ocean’s real gems.
For most of us, restricted to roaming the shoreline, sea slugs are a rare find—if we recognise them at all. Yet on odd occasions a few species become briefly abundant. I vividly recall in the mid-1960s finding a multitude of sea hares—a type of sea slug—on the wide rock platform that runs from just beyond Te Araroa out towards East Cape. Each the length of a finger, they were mottled seaweed brown in colour and released a purple dye when disturbed. There were at least 10 to the square metre in a band 50 m wide and 5 or 10 km long. Prior to that encounter, I could count on the fingers of one hand the number of sea hares I’d spotted. Suddenly, here were millions of them, probably involved in a midsummer orgy of mating and egg-laying. Within a week or two they would probably have died.
By definition, slugs lack shells, but what do you call something that has a small vestigial shell somewhere in its internals? It’s this kind of problem that complicates the taxonomy of marine slugs. Formally, they are gastropod molluscs, members of the subclass Opisthobranchia (from Greek, meaning rear-gilled, pronounced er-pissth-er-brank-ee-er), all of whose members show some reduction of the shell. But there are five orders of opisthobranch, among which are species with shells of quite respectable size (e.g. bubble shells) while others lack shells entirely. There are also plenty of intermediate forms. All have a minute shell at an early stage of their development, but members of the order Nudibranchia (the name means bare gilled, nude-ee-brank-ee-er) lose it completely, whereas sea hares retain a small internal shell.
There are other differences between the groups. Nudibranchs—our main focus—either carry a bunch of flowery gills on their back if they are dorids or have the look of free-living eyebrows if they are aeolids, the other major type of nudibranch. Both groups are carnivores. Sea hares (order Anaspidea) have concealed gills and are herbivores. The members of another order, Sacoglossa, are specialised herbivores.
Just to complicate matters, there are a few marine slugs that are not closely related to any of these main groups. A very solid, 12-cm long black slug is sometimes found on rocks at low tide. Prod it in the middle of the back and a slit of white shell becomes visible. This is the shield shell, Scutus breviculus, a relative of limpets and abalone that resembles a shell-less paua. In the higher reaches of the intertidal zone, a 2 cm leathery, mottled, dark-grey slug, Onchidella nigricans, is often to be seen inconspicuously clinging to rocks. This is an air breather, in the same group of molluscs as terrestrial slugs and only a distant relative of the true sea slugs.
No sea slugs occur in fresh water, but they are widely distributed in the ocean, being found from the Antarctic (where many species seem to be white or colourless) to the tropics. Some species float on the surface of the sea, and one has been recovered from beside a deep-ocean hydrothermal vent. However, most frequent the shallows of temperate and tropical seas on solid substrates. Worldwide there are perhaps 3000 opisthobranch species, of which more than 130 are found in New Zealand waters, including more than 90 described nudibranchs, eight sea hares and seven sacoglossans. Of these, 76 are found only around our coasts, 19 also dwell in eastern Australian seas and 39 are distributed more widely around the south-west Pacific.
This high degree of local endemism is a little surprising, since most newly hatched sea slugs undergo a month-long veliger (or free-swimming larval) stage in the plankton, during which currents can disperse them very widely.
Quite a number of richly coloured species of tropical origin have been discovered in northern New Zealand waters over the last 30 years (e.g. members of the genus Tambja). These presumably arrived as veligers and found the living congenial once they had settled. Since currents flow down the east coast of Australia, across the Tasman and along the east coast of New Zealand, it is relatively easy for sea slugs from the north-west to arrive here. For species originating in our waters, there is no landfall to be made to the east until South America, and most veligers cannot last a Pacific crossing. We are the end of the line.
Sea slugs—especially nudibranchs—have a num-ber of claims to fame. Beauty of colour and form is only the beginning. Perhaps, in all nature, sea slugs are the ultimate recyclers. Where do all those brilliant colours come from? Many are lifted straight from their food. Where do their defences come from? Again, most are ingenious redeployments of materials they have ingested. And many species put other elements of their food to work for them in a most clever and unusual manner.
Why do nudibranchs resort to such measures? Imagine an oyster, scallop or paua, its shell cast aside, living as an unprotected organism on the sea floor. It wouldn’t last a minute. Yet this apparently suicidal path is the route sea slugs have chosen. Having thrown aside the fetters and protection of a shell, they have had to adopt other means of self-preservation.
For many, camouflage is the first line of defence. Their bright colours and bold patterns make them inconspicuous among the equally bright sponges, soft corals and bryozoans they generally feed upon. Some take the pigments from the sponges they eat and display them directly in their own skin, although many species synthesise their own colours. Others opt for a translucent skin and let the colour of the contents of their digestive system show through. More impressively, many species seem to have acquired the ability to feed on organisms eschewed by other predators because of their toxicity. Not only do they somehow avoid being harmed by the toxins, but they are able to incorporate the poisons in their own tissues to discourage would-be predators.
This habit is not restricted to the carnivorous nudibranchs. Sacoglossans eat toxic seaweeds, storing noxious diterpene derivatives for their own use. When disturbed or attacked, they quickly release copious amounts of diterpene-laced mucus, while their egg masses are seasoned likewise.
The skin of sea hares contains toxic compounds from the red algae they graze upon. One Western Australian species, Aplysia gigantea, has caused the death of a number of dogs which have ingested it. Typically, fish will quickly spit out a sea slug they have gobbled up and eschew such fare in future.
A sea slug’s toxins do not all come directly from its food, however. Some are the result of post-prandial modification, while others, such as polypropionates, are synthesised de novo.
Some slugs, such as the members of the family Chromodorididae are so confident of their unpalatability that they shrug off camouflage, opting instead for bold, warning flamboyance, termed aposematic colouration. Glands in the mantle accumulate poisonous and repugnant chemicals drawn from the sponges they feed on, and it is thought that in linking bright colours with bad taste, the slugs are in effect trying to educate fish to leave them alone. Some unrelated non-toxic invertebrates, such as flatworms and sea cucumber, mimic the colours of certain slugs, hoping to gain protection from their pariah status.
Aeolids, one of the two main types of nudibranch, have perfected a much more elaborate sleight of hand. They are slender, elegant creatures, distinguished by the many long dreadlock-like projections that adorn their backs, called cerata (singular: ceras). Cerata are blood-filled tubes that greatly increase the surface area used for gas exchange, allowing aeolids to do without gills. Although cerata are typically of a brown or reddish colour, the epithelium that encases them is transparent and much of the colour comes from food within the large digestive gland, a vast organ that sends a lobe up every ceras.
Aeolids feed on cnidarians—the group that includes hydroids, corals, anemones and jellyfish. Many of these are equipped with stinging cells (nematocysts) for food capture and self-defence. Somehow, aeolids can chew through cnidarians without discharging all the nematocysts and without suffering serious harm from those they do. More than that, they can then separate undischarged nematocysts from other components of a meal and shuffle these biological hand grenades to the tips of their cerata. It has been suggested that the nematocysts slugs capture in this way are not fully mature, and that they become so only once they have been consumed. Careful examination of the tip of each ceras reveals a small white dot—the cnidosac—where the nematocysts are stored at the end of the finger of gut. The nematocysts in the cnidosac remain functional, and any attack on the ceras triggers their discharge.
Perhaps the finest exponent of this method of defence is Glaucus atlanticus, which is found in many of the world’s warmer seas, including those around northern New Zealand. G. atlanticus feeds on the Portuguese man-of-war (a surface-floater like itself) and stores the extremely potent jellyfish nematocysts in its cerata. If handled by a diver or beachcomber, this beautiful slug can administer a sting as painful as that given by a man-of-war.
At the other extreme of the potency spectrum are nematocysts from some soft corals. These are so mild that, as far as the aeolids that prey upon them are concerned, they are of little use. In these species—members of the genus Phyllodesmium, for example (including P. magnum, found around the Kermadec Islands)—cnidosacs are often replaced by large glands that secrete sticky mucus. Phyllodesmium species can also shed cerata, which then writhe about, perhaps so bemusing predators that the slugs can make a sedate escape. Cerata can be regenerated, so the loss is not permanent.
Bill Rudman, a New Zealander at the Australian Museum in Sydney and an authority on opisthobranchs, has speculated that the cnidosac may not be as clever an adaptation as it seems. Rather than being the ultimate in sophisticated recycled defence, he suggests, it may simply be a means of getting rid of some of the unpleasant bits in a slug’s food.
We are not yet finished with the remarkable capacity of nudibranchs to make the most of their meals. Living within the tissues of many cnidarians—most famously the polyps of reef-building corals—are single-celled algae called zooxanthellae. Host and lodger live symbiotically: the animals provide the algae with physical protection from the elements while allowing them exposure to sunlight and bathing them in carbon dioxide from their metabolism; thus supplied, the algae photosynthesise more than enough energy for their modest needs, and the excess flows to the host.
In recent years widespread coral bleaching has been noticed in many tropical reefs, caused by the eviction of zooxanthellae from the host polyps once water temperatures have risen to 33° C. This act of inhospitality is thought to be bad for reefs, and in some cases presages death for the coral.
Zooxanthellae—of which there are many species—don’t just live in coral polyps, however. They also inhabit, among others, sea anemones, giant clams and even some protists (minute single-celled organisms), such as foraminifera and radiolarians. Consequently many sea slugs acquire them from their food, but, instead of simply digesting them, they put the algae to work in their own tissues. Presumably this reduces the slugs’ food requirements.
Sacoglossans go a step further. The radula—a ribbon of teeth possessed by all gastropods—of a sacoglossan boasts particularly fine, sharp gnashers like miniature stilettos, which the herbivore slug uses to slice open the cells of algae before sucking their contents into its mouth and passing them to its digestive gland. Some species contrive to separate out the plastids and chloroplasts—the plant organs responsible for photosynthesis—and sequester them intact and functioning in those parts of their bodies that are well exposed to light, such as pseudo-cerata along their backs. It is these purloined chloroplasts that give many sacoglossans their green colour. (Incidentally, there is a name for the misappropriation of chloroplasts—kleptoplasty.)
In one way or another, therefore, quite a few sea slugs carry solar panels on their backs that reduce their dependence on outside food supplies.
A certain zaniness infuses the way that sea slugs carry on some of the other day-to-day basics of life. Take reproduction. All sea slugs are hermaphrodites, endowed with both male and female reproductive tissues and organs. However, they never self-fertilise but pair up head to tail, both fertilising and being fertilised simultaneously via openings on the right side of the body. In some species, partners fire packets of sperm into each other’s body, and older individuals can carry scars from the experience. Mating may take seconds or last for days, depending on the species. Sea hares indulge in group sex, forming chains of mating animals. Fertilised eggs are usually minute coloured blobs encased within a ribbon of jelly that attaches to a solid surface. Typically there are thousands of eggs per ribbon, in some species as many as a million or more.
A peptide pheromone—attractin, the first water-borne pheromone found in an invertebrate—has been isolated from the egg masses of sea hares. It is this that draws animals to sites of reproductive activity.
The egg ribbons are generally laid in a coil, and there has been speculation as to whether the coils of Northern-hemisphere sea slugs curl in the opposite direction from those of Southern-hemisphere slugs. In most species, it seems that the slug starts in the centre and lays in an anticlockwise direction. In a few the ribbon spirals the other way, but it is possible that in these cases the eggs are laid from the outside in—which means the slug would still be moving anticlockwise. So far there is little evidence for the notion of different directions in different hemispheres.
Eggs hatch into tiny-shelled veligers, which in most species drift for a month or so in the plankton. During this sojourn mortality is very high, but the survivors settle down, for the most part jettison their shells, and start to grow. If, after the month, they are unable to find a suitable substrate to settle on, they can remain in the plankton for a few more weeks. Others skip the planktonic OE or have only a short larval phase.
And here is an arcane morsel of trivia. The element strontium is essential both for calcification of the embryonic shell and the formation of granules inside statocysts, organs which animals use to detect gravity. By depriving developing veligers of strontium, experimenters have produced sea slugs that are neurologically defective and unable to orientate with respect to gravity. Apparently they are useful for studying neural architecture and behavioural reactions to seeming weightlessness.
In a few overseas species whose life histories have been studied, slugs become sexually mature 21–50 days after settling and live for 3–12 months in total. That said, a species of sea hare which survives for a year in the wild has been found to live for six years in aquaria. Some of the short-lived species are probably driven by the need to complete their life cycle before the colony of hydroids or sponges they live upon dies and they starve without having bred.
Incidentally, large aggregations are not all caused by slugs coming together for reproduction. Exceptional settlement and survival followed by rapid growth because of an abundance of food explain some large aggregations of slugs.
Sea slugs crawl in much the same manner as terrestrial slugs and marine snails—generally through backward waves of contraction passing along the sole of the animal’s foot, propelling it forward. As slugs on land leave a trail of slime, so do those in the sea. When moving over difficult terrain, such as the lacy branches of bryozoans, some species secrete an especially sticky mucus that aids adhesion between foot and substrate. But a mucus trail is also a path that can be followed by those with evil intent. Although sea slugs seem to have few predators, some species of slug prey on other slugs, and they can find them by following their trails. In the Poor Knights Islands, the large gold-lined nudibranch Roboastra luteolineata has been seen to devour the not much smaller Verco’s nudibranch, Tambja verconis. The predator’s everted oral tube and buccal bulb extend to engulf its prey, which is gradually swallowed whole. Sometimes slugs of the same species seem to follow one another about, presumably again by sticking to slime trails.
Humans also pursue slugs, sometimes with more than photography in mind. Sea hares belonging to the genus Aplysia have been important model organisms for neurophysiological investigation over the last 20 years. Their brains are simple but are constructed from extremely large nerve cells that can be individually mapped. Nudibranch eyes are rudimentary, buried below the skin and capable only of discerning variations in light levels, so little in the way of brain power is needed for visual processing. However, the sense of smell is important and operates via club-shaped rhinophores carried atop the head. Aplysia slugs are also capable of simple learning, and changes in the ganglia of animals that have learned something—such as to move to avoid an uncomfortable stimulus—can be compared with those of naïve animals.
Given their baggage of distasteful and toxic ingredients, sea slugs are not much sought after for human gastronomy—and best avoided if encountered on a plate—but there is interest in them as sources of cytotoxic compounds (poisonous to living cells) for fighting microbes and cancer. From the sea hare Dolabella auricularia, five cytotoxic glycoproteins showing antimicrobial activity, and named dolabellanins A, C, E, P and B2, have been isolated, as well as several different peptides, called dolastatins, which have potential as anti-cancer drugs. It is now thought that the dolastatins are derived from cyanobacteria (containing blue photosynthetic pigment) ingested by the sea hares. Many more such compounds no doubt await discovery.
While most sea slugs are smallish—30–100 mm long—a few species grow much larger. Several nudibranchs reach 300–500 mm in length (think of a large pizza, because at least some such species are circular or oval in shape), but these are dwarfed by the Californian sea hare Aplysia vaccaria, which is reported to reach a metre in length and weigh 14 kg. Not a slug to be taken lightly.